Skip to main content
SpringerLink
Log in

Sensory Integration, Sensory Processing, and Sensory Modulation Disorders: Putative Functional Neuroanatomic Underpinnings

  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

This paper examines conditions that have variously been called sensory integration disorder, sensory processing disorder, and sensory modulation disorder (SID/SPD/SMD). As these conditions lack readily and consistently agreed-upon operational definitions, there has been confusion as to how these disorders are conceptualized. Rather than addressing various diagnostic controversies, we will instead focus upon explaining the symptoms that are believed to characterize these disorders. First, to clarify the overall context within which to view symptoms, we summarize a paradigm of adaptation characterized by continuous sensorimotor interaction with the environment. Next, we review a dual-tiered, integrated model of brain function in order to establish neuroanatomic underpinnings with which to conceptualize the symptom presentations. Generally accepted functions of the neocortex, basal ganglia, and cerebellum are described to illustrate how interactions between these brain regions generate both adaptive and pathological symptoms and behaviors. We then examine the symptoms of SID/SPD/SMD within this interactive model and in relation to their impact upon the development of inhibitory control, working memory, academic skill development, and behavioral automation. We present likely etiologies for these symptoms, not only as they drive neurodevelopmental pathologies but also as they can be understood as variations in the development of neural networks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Ayres AJ. Sensory integration and the child. Los Angeles: Western Psychological Services; 2005.

    Google Scholar 

  2. Ayres AJ. Types of sensory integrative dysfunction among disabled learners. Am J Occup Ther. 1972;26(1):13–8.

    PubMed  CAS  Google Scholar 

  3. Bar-Shalita T, Vatine JJ, Seltzer Z, Parush S. Psychophysical correlates in children with sensory modulation disorder (SMD). Physiol Behav. 2009;98(5):631–9.

    Article  PubMed  CAS  Google Scholar 

  4. Dunn W. The Sensory Profile: a discriminating measure of sensory processing in daily life. Sens Integr Spec Interest Sect Q. 1997;20(1):1–3.

    Google Scholar 

  5. Zero to Three (Organization). DC:0-3R: diagnostic classification of mental health and developmental disorders of infancy and early childhood. Washington, DC: Zero To Three; 2005.

    Google Scholar 

  6. Hertza J, Estes B. Developmental dyspraxia and developmental coordination disorder. In: Davis AS, editor. Handbook of pediatric neuropsychology. New York: Springer; 2011. p. 593–602.

    Google Scholar 

  7. James K, Miller LJ, Schaaf R, Nielsen DM, Schoen SA. Phenotypes within sensory modulation dysfunction. Comprehensive Psychiatry; 2011.

  8. Koziol LF, Budding DE. Subcortical structures and cognition: implications for neuropsychological assessment. New York: Springer; 2009.

    Google Scholar 

  9. Cisek P, Kalaska JF. Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci. 2010;33:269–98.

    Article  PubMed  CAS  Google Scholar 

  10. Shadlen MN, Movshon JA. Synchrony unbound: review. A critical evaluation of the temporal binding hypothesis. Neuron. 1999;24:67–77.

    Article  PubMed  CAS  Google Scholar 

  11. Singer W. Consciousness and the binding problem. Ann NY Acad Sci. 2001;929(1):123–46.

    Article  PubMed  CAS  Google Scholar 

  12. Cisek P, Puskas GA, El-Murr S. Decisions in changing conditions: the urgency-gating model. J Neurosci. 2009;29(37):11560–71.

    Article  PubMed  CAS  Google Scholar 

  13. Cisek P. Cortical mechanisms of action selection: the affordance competition hypothesis. Philos Trans R Soc Lond B Biol Sci. 2007;362(1485):1585–99.

    Article  PubMed  Google Scholar 

  14. Pezzulo G, Barsalou LW, Cangelosi A, Fischer MH, McRae K, Spivey MJ. The mechanics of embodiment: a dialog on embodiment and computational modeling. Frontiers in Psychology. 2011;2.

  15. Milner AD, Goodale MA. Two visual systems re-viewed. Neuropsychologia. 2008;46(3):774–85.

    Article  PubMed  CAS  Google Scholar 

  16. Barsalou LW. Grounded cognition. Annu Rev Psychol. 2008;59:617–45.

    Article  PubMed  Google Scholar 

  17. Njiokiktjien C. Developmental dyspraxias: assessment and differential diagnosis. In: Riva D, Njiokiktjien C, editors. Brain lesion localization and developmental functions. Montrouge, France: John Libbey Eurotext; 2010. p. 157–86.

  18. Sheth SA, Abuelem T, Gale JT, Eskandar EN. Basal ganglia neurons dynamically facilitate exploration during associative learning. J Neurosci. 2011;31(13):4878.

    Article  PubMed  CAS  Google Scholar 

  19. Cisek P, Kalaska JF. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron. 2005;45(5):801–14.

    Article  PubMed  CAS  Google Scholar 

  20. Baranek GT. Efficacy of sensory and motor interventions for children with autism. J Autism Dev Disord. 2002;32(5):397–422.

    Article  PubMed  Google Scholar 

  21. Schaaf RC, Davies PL. Evolution of the sensory integration frame of reference. Am J Occup Ther. 2010;64(3):363–7.

    Article  PubMed  Google Scholar 

  22. Reynolds S, Lane S. Diagnostic validity of sensory over-responsivity: a review of the literature and case reports. J Autism Dev Disord. 2008;38(3):516–29.

    Article  PubMed  Google Scholar 

  23. Wiggins LD, Robins DL, Bakeman R, Adamson LB. Brief report: sensory abnormalities as distinguishing symptoms of autism spectrum disorders in young children. J Autism Dev Disord. 2009;39(7):1087–91.

    Article  PubMed  Google Scholar 

  24. Reynolds S, Lane SJ. Sensory overresponsivity and anxiety in children with ADHD. Am J Occup Ther. 2009;63(4):433.

    Article  PubMed  Google Scholar 

  25. Boyd BA, Baranek GT, Sideris J, Poe MD, Watson LR, Patten E, et al. Sensory features and repetitive behaviors in children with autism and developmental delays. Autism Res. 2010;3(2):78–87.

    PubMed  Google Scholar 

  26. Baranek GT, Boyd BA, Poe MD, David FJ, Watson LR. Hyperresponsive sensory patterns in young children with autism, developmental delay, and typical development. Am J Ment Retard. 2007;112(4):233–45.

    Article  PubMed  Google Scholar 

  27. Cascio CJ. Somatosensory processing in neurodevelopmental disorders. Journal of Neurodevelopmental Disorders. 2010;2(2):62–9.

    Article  Google Scholar 

  28. Levisohn L, Cronin-Golomb A, Schmahmann JD. Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain. 2000;123(Pt 5):1041–50.

    Article  PubMed  Google Scholar 

  29. Tavano A, Borgatti R. Evidence for a link among cognition, language and emotion in cerebellar malformations. Cortex. 2007;46(7):907–18.

    Article  Google Scholar 

  30. Green D, Baird G, Sugden D. A pilot study of psychopathology in developmental coordination disorder. Child Care Health Dev. 2006;32(6):741–50.

    Article  PubMed  CAS  Google Scholar 

  31. Zwicker JG, Missiuna C, Boyd LA. Neural correlates of developmental coordination disorder: a review of hypotheses. J Child Neurol. 2009;24(10):1273.

    Article  PubMed  Google Scholar 

  32. Marien P, Wackenier P, De Surgeloose D, De Deyn PP, Verhoeven J. Developmental coordination disorder: disruption of the cerebello-cerebral network evidenced by SPECT. The Cerebellum. 2010;1–6.

  33. Davies PL, Gavin WJ. Validating the diagnosis of sensory processing disorders using EEG technology. Am J Occup Ther. 2007;61(2):176–89.

    Article  PubMed  Google Scholar 

  34. Schaaf RC, Benevides T, Blanche EI, Brett-Green BA, Burke JP, Cohn ES, et al. Parasympathetic functions in children with sensory processing disorder. Front Integr Neurosci. 2010;4:4.

    Article  PubMed  Google Scholar 

  35. Schoen SA, Miller LJ, Brett-Green BA, Nielsen DM. Physiological and behavioral differences in sensory processing: a comparison of children with autism spectrum disorder and sensory modulation disorder. Frontiers in Integrative Neuroscience 2009;3.

  36. Schoen SA, Miller LJ, Brett-Green B, Reynolds S, Lane SJ. Arousal and reactivity in children with sensory processing disorder and autism spectrum disorder. Psychophysiology 2008;45.

  37. Mangeot SD, Miller LJ, McIntosh DN, McGrath-Clarke J, Simon J, Hagerman RJ, et al. Sensory modulation dysfunction in children with attention-deficit–hyperactivity disorder. Dev Med Child Neurol. 2001;43(6):399–406.

    Article  PubMed  CAS  Google Scholar 

  38. Ognibene TC. Distinguishing sensory modulation dysfunction from attention-deficit/hyperactivity disorder: sensory habituation and response inhibition processes. University of Denver; 2002.

  39. Goddard S, Blythe SG, Beuret LJ, Blythe P. Attention, balance, and coordination: the ABC of learning success. Wiley; 2009.

  40. Marco EJ, Hinkley LBN, Hill SS, Nagarajan SS. Sensory processing in autism: a review of neurophysiologic findings. Pediatric Research; 2011.

  41. Bargh JA, Chartrand TL. The unbearable automaticity of being. Social cognition: key readings. 2005;228.

  42. Bargh, J. A. The automaticity of everyday life. In: Wyer, RS, editor. The automaticity of everyday life: Advances in social cognition, vol. 10. Mahwah, NJ: Erlbaum Associates; 1997. p. 1-61.

    Google Scholar 

  43. Hikosaka O, Isoda M. Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms. Trends Cogn Sci. 2010;14(4):154–61.

    Article  PubMed  Google Scholar 

  44. Ashby FG, Turner BO, Horvitz JC. Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci. 2010;14(5):208–15.

    Article  PubMed  Google Scholar 

  45. Toates F. A model of the hierarchy of behaviour, cognition, and consciousness. Conscious Cogn. 2006;15(1):75–118.

    Article  PubMed  Google Scholar 

  46. Restivo L, Frankland PW. Shifting to automatic. Frontiers in Integrative Neuroscience. 2010;4 (doi: 10.3389/neuro.07.001.2010).

  47. Podell K, Lovell M, Goldberg E. Lateralization of frontal lobe functions. In: Salloway SP, Malloy PF, Duffy JD, editors. The frontal lobes and neuropsychiatric illness. Washington, DC: American Psychiatric; 2001. p. 83–100.

    Google Scholar 

  48. Goldberg E, Bilder RM. The frontal lobes and hierarchical organization of cognitive control. The frontal lobes revisited. 1987;159–87.

  49. Goldberg E, Costa LD. Qualitative indices in neuropsychological assessment: an extension of Luria’s approach to executive deficit following prefrontal lesions. Neuropsychological assessment of neuropsychiatric disorders. 1986;48–64.

  50. Kinsbourne M. Development of attention and metacognition. In: Rapin I, Segalowitz SJ, editors. Handbook of neuropsychology, vol. 7. Amsterdam: Elsevier; 1993. p. 261–78.

    Google Scholar 

  51. Marcovitch S, Zelazo PD. A hierarchical competing systems model of the emergence and early development of executive function. Dev Sci. 2009;12(1):1–18.

    Article  PubMed  Google Scholar 

  52. de Quiros JB, Schrager OL. Neuropsychological fundamentals in learning disabilities. Academic Therapy Publications; 1978.

  53. Piek JP. Infant motor development. Human Kinetics; 2006.

  54. Redgrave P, Prescott TJ, Gurney K. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience. 1999;89(4):1009–23.

    Article  PubMed  CAS  Google Scholar 

  55. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, et al. Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nature Reviews Neuroscience; 2010.

  56. Reiner A. The conservative evolution of the vertebrate basal ganglia. Handbook of basal ganglia structure and function. 2010;29–62.

  57. Reiner A. You cannot have a vertebrate brain without a basal ganglia. The basal ganglia IX. 2009;3–24.

  58. Frank MJ, Scheres A, Sherman SJ. Understanding decision-making deficits in neurological conditions: insights from models of natural action selection. Philos Trans R Soc Lond B Biol Sci. 2007;362(1485):1641–54.

    Article  PubMed  Google Scholar 

  59. Graybiel AM. The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem. 1998;70(1–2):119–36.

    Article  PubMed  CAS  Google Scholar 

  60. Graybiel AM, Aosaki T, Flaherty AW, Kimura M. The basal ganglia and adaptive motor control. Science. 1994;265(5180):1826.

    Article  PubMed  CAS  Google Scholar 

  61. Doyon J, Ungerleider LG. Functional anatomy of motor skill learning. In: Squire LR, editor. Neuropsychology of memory. New York: Guilford; 2002. p. 225–38.

    Google Scholar 

  62. Humphries MD, Prescott TJ. The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog Neurobiol. 2010;90(4):385–417.

    Article  PubMed  Google Scholar 

  63. Squire LR. Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem. 2004;82(3):171–7.

    Article  PubMed  Google Scholar 

  64. Knowlton BJ. The role of the basal ganglia in learning and memory. In: Squire LR, Schacter DL, editors. The neuropsychology of memory. 3rd ed. New York: Guilford; 2002. p. 143–53.

    Google Scholar 

  65. Corbit LH, Janak PH. Posterior dorsomedial striatum is critical for both selective instrumental and Pavlovian reward learning. Eur J Neurosci. 2010;31(7):1312–21.

    Article  PubMed  Google Scholar 

  66. Schwartze M, Keller PE, Patel AD, Kotz SA. The impact of basal ganglia lesions on sensorimotor synchronization, spontaneous motor tempo, and the detection of tempo changes. Behav Brain Res. 2011;216(2):685–91.

    Article  PubMed  Google Scholar 

  67. Doll BB, Frank MJ. The basal ganglia in reward and decision making: computational models and empirical studies. Handbook of Reward and Decision Making. 2009;399:399–425.

    Article  Google Scholar 

  68. Schwabe L, Wolf OT. Stress-induced modulation of instrumental behavior: from goal-directed to habitual control of action. Behavioural Brain Research; 2010 (in press).

  69. Fuster JM. The prefrontal cortex. Academic; 2008.

  70. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986;9:357–81.

    Article  PubMed  CAS  Google Scholar 

  71. Middleton FA, Strick PL. A revised neuroanatomy of frontal–subcortical circuits. Frontal–subcortical circuits in psychiatric and neurological disorders. 2001;44–58.

  72. Seger CA, Miller EK. Category learning in the brain. Annual Review of Neuroscience. 2010;33(1).

  73. Bonelli RM, Cummings JL. Frontal–subcortical circuitry and behavior. Dialogues Clin Neurosci. 2007;9(2):141.

    PubMed  Google Scholar 

  74. Cummings JL. Anatomic and behavioral aspects of frontal–subcortical circuits. Ann NY Acad Sci. 1995;769(1):1–13.

    Article  PubMed  CAS  Google Scholar 

  75. Lichter DG, Cummings JL. Frontal–subcortical circuits in psychiatric and neurological disorders. Guilford; 2001.

  76. Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2010;35(1):4–26.

    Article  PubMed  Google Scholar 

  77. Marsh R, Maia TV, Peterson BS. Functional disturbances within frontostriatal circuits across multiple childhood psychopathologies. Am J Psychiatry. 2009;166(6):664–74.

    Article  PubMed  Google Scholar 

  78. Smeets WJ, Marin O, Gonzalez A. Evolution of the basal ganglia: new perspectives through a comparative approach. J Anat. 2000;196:501–17.

    Article  PubMed  CAS  Google Scholar 

  79. Striedter GF. Principles of brain evolution. New York: Sinauer; 2005.

    Google Scholar 

  80. Erbetta A. Basal ganglia and thalamus: connections and functions. In: Riva D, Njiokiktjien C, editors. Brain lesion localization and developmental functions. Montrouge, France: John Libbey Eurotext; 2010. p. 11–6.

  81. McHaffie JG, Stanford TR, Stein BE, Coizet V, Redgrave P. Subcortical loops through the basal ganglia. Trends Neurosci. 2005;28(8):401–7.

    Article  PubMed  CAS  Google Scholar 

  82. Miller R. A theory of the basal ganglia and their disorders. Boca Raton: CRC; 2008.

    Google Scholar 

  83. Redgrave P, Coizet V, Comoli E, McHaffie JG, Leriche M, Vautrelle N, et al. Interactions between the midbrain superior colliculus and the basal ganglia. Frontiers in Neuroanatomy. 2010;4.

  84. Winn P, Wilson DIG, Redgrave P. Subcortical connections of the basal ganglia. Handbook Of Behavioral Neuroscience. 2010;20:397–408.

    Article  Google Scholar 

  85. Desrochers TM, Jin DZ, Goodman ND, Graybiel AM. Optimal habits can develop spontaneously through sensitivity to local cost. Proc Natl Acad Sci. 2010;107(47):20512–7.

    Article  PubMed  CAS  Google Scholar 

  86. Wilson DIG, MacLaren DAA, Winn P. On the relationships between the pedunculopontine tegmental nucleus, corticostriatal architecture, and the medial reticular formation. The basal ganglia IX. 2009;143.

  87. Sarvestani IK, Lindahl M, Hellgren-Kotaleski J, Ekeberg +. The arbitration–extension hypothesis: a hierarchical interpretation of the functional organization of the basal ganglia. Frontiers in Systems Neuroscience. 2011;5.

  88. Hoshi E, Tremblay L, Feger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8(11):1491–3.

    Article  PubMed  CAS  Google Scholar 

  89. Bostan AC, Dum RP, Strick PL. The basal ganglia communicate with the cerebellum. Proceedings of the National Academy of Sciences. 2010.

  90. Durston S, Belle JV, Zeeuw PD. Differentiating frontostriatal and fronto-cerebellar circuits in attention-deficit/hyperactivity disorder. Biol Psychiatry 2010.

  91. Mendoza J, Foundas AL. Clinical neuroanatomy: a neurobehavioral approach. Springer; 2007.

  92. Glickstein M, Strata P, Voogd J. Cerebellum: history. Neuroscience. 2009;162(3):549–59.

    Article  PubMed  CAS  Google Scholar 

  93. Glickstein M, Sultan F, Voogd J. Functional localization in the cerebellum. Cortex. 2011;47(1):59–80.

    Article  PubMed  Google Scholar 

  94. Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M. Modular organization of internal models of tools in the human cerebellum. Proc Natl Acad Sci USA. 2003;100(9):5461–6.

    Article  PubMed  CAS  Google Scholar 

  95. Schmahmann JD. The cerebellum and cognition. Academic; 1997.

  96. Schmahmann JD. Rediscovery of an early concept. Int Rev Neurobiol. 1997;41:3–27.

    Article  PubMed  CAS  Google Scholar 

  97. Cerminara NL, Apps R. Behavioural significance of cerebellar modules. The Cerebellum 2010;1–11.

  98. Ghelarducci B. The cerebellum as a multipurpose neural machine: basic principles and future perspectives. In: Riva D, Njiokiktjien C, editors. Brain lesion localization and developmental functions. Montrouge: Libbey Eurotext; 2010. p. 111–32.

    Google Scholar 

  99. Bower JM. Control of sensory data acquisition. Int Rev Neurobiol. 1997;41:489–513.

    Article  PubMed  CAS  Google Scholar 

  100. Manto M, Nowak DA, Schutter DJ. Coupling between cerebellar hemispheres and sensory processing. Cerebellum. 2006;5(3):187–8.

    Article  PubMed  Google Scholar 

  101. Molinari M, Chiricozzi FR, Clausi S, Tedesco AM, De LM, Leggio MG. Cerebellum and detection of sequences, from perception to cognition. Cerebellum. 2008;7(4):611–5.

    Article  PubMed  Google Scholar 

  102. Bower JM, Kassel J. Variability in tactile projection patterns to cerebellar folia crus IIA of the Norway rat. J Comp Neurol. 1990;302(4):768–78.

    Article  PubMed  CAS  Google Scholar 

  103. Montgomery J, Bodznick D. Functional origins of the vertebrate cerebellum from a sensory processing antecedent. Curr Zool Current Zoology. 2010;56(3):277–84.

    Google Scholar 

  104. Balsters JH, Ramnani N. Cerebellar plasticity and the automation of first-order rules. J Neurosci. 2011;31(6):2305–12.

    Article  PubMed  CAS  Google Scholar 

  105. Thach WT. Context-response linkage. In: Schmahmann J, editor. The cerebellum and cognition. San Diego: Academic; 1997. p. 600–12.

    Google Scholar 

  106. Bloedel JR, Bracha V. Duality of cerebellar motor and cognitive functions. Int Rev Neurobiol. 1997;41:613.

    Article  PubMed  CAS  Google Scholar 

  107. Akshoomoff NA, Courchesne E, Townsend J. Attention coordination and anticipatory control. In: Schmahmann J, editor. The cerebellum and cognition. San Diego: Academic; 1997. p. 575–600.

    Google Scholar 

  108. Schmahmann JD, Pandya DN. The cerebrocerebellar system. Int Rev Neurobiol. 1997;41:31–60.

    Article  PubMed  CAS  Google Scholar 

  109. Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.

    Article  PubMed  CAS  Google Scholar 

  110. Krienen FM, Buckner RL. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex. 2009;19(10):2485–97.

    Article  PubMed  Google Scholar 

  111. Ito M. Cerebellar microcomplexes. Int Rev Neurobiol. 1997;41:475–87.

    Article  PubMed  CAS  Google Scholar 

  112. Zhu JN, Wang JJ. The cerebellum in feeding control: possible function and mechanism. Cell Mol Neurobiol. 2008;28(4):469–78.

    Article  PubMed  Google Scholar 

  113. Zhu JN, Yung WH, Kwok-Chong CB, Chan YS, Wang JJ. The cerebellar–hypothalamic circuits: potential pathways underlying cerebellar involvement in somatic–visceral integration. Brain Res Rev. 2006;52(1):93–106.

    Article  PubMed  Google Scholar 

  114. Schmahmann JD. The cerebrocerebellar system: anatomic substrates of the cerebellar contribution to cognition and emotion. Int Rev Psychiatry. 2001;13(4):247–60.

    Article  Google Scholar 

  115. Schmahmann JD, Caplan D. Cognition, emotion and the cerebellum. Brain. 2006;129(Pt 2):290–2.

    PubMed  Google Scholar 

  116. Leiner HC, Leiner AL. How fibers subserve computing capabilities: similarities between brains and machines. Int Rev Neurobiol. 1997;41:535–53.

    Article  PubMed  CAS  Google Scholar 

  117. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.

    Article  PubMed  CAS  Google Scholar 

  118. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.

    Article  PubMed  CAS  Google Scholar 

  119. Ito M. Bases and implications of learning in the cerebellum—adaptive control and internal model mechanism. Prog Brain Res. 2005;148:95–109.

    Article  PubMed  Google Scholar 

  120. Galea JM, Vazquez A, Pasricha N, Orban de Xivry JJ, Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cerebral Cortex 2010.

  121. Saling LL, Phillips JG. Automatic behaviour: efficient not mindless. Brain Res Bull. 2007;73(1–3):1–20.

    Article  PubMed  CAS  Google Scholar 

  122. Dietrichs E. Clinical manifestation of focal cerebellar disease as related to the organization of neural pathways. Acta Neurol Scand Suppl. 2008;188:6–11.

    Article  PubMed  CAS  Google Scholar 

  123. Manto MU. On the cerebello–cerebral interactions. Cerebellum. 2006;5(4):286–8.

    Article  PubMed  Google Scholar 

  124. Zheng N, Raman IM. Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei. Cerebellum. 2010;9(1):56–66.

    Article  PubMed  Google Scholar 

  125. Manto M, Oulad Ben Taib N. Cerebellar nuclei: key roles for strategically located structures. Cerebellum. 2010;9(1):17–21.

    Article  PubMed  Google Scholar 

  126. Ramnani N. The primate cortico–cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7(7):511–22.

    Article  PubMed  CAS  Google Scholar 

  127. Schmahmann JD. The role of the cerebellum in affect and psychosis. J Neurolinguist. 2000;13(2–3):189–214.

    Article  Google Scholar 

  128. Tavano A, Borgatti R. Evidence for a link among cognition, language and emotion in cerebellar malformations. Cortex. 2010;46(7):907–18.

    Article  PubMed  Google Scholar 

  129. Galliano E, Mazzarello P, D’Angelo E. Discovery and rediscoveries of Golgi cells. J Physiol. 2010;588(Pt 19):3639–55.

    Article  PubMed  CAS  Google Scholar 

  130. D′Angelo E, Mazzarello P, Prestori F, Mapelli J, Solinas S, Lombardo P, et al. The cerebellar network: from structure to function and dynamics. Brain Res Rev. 2010; Oct 13.

  131. Houk JC, Mugnaini E. Cerebellum. Fundamental neuroscience. Amsterdam: Elsevier; 2003. p. 841–72.

  132. Ausim Azizi S. And the olive said to the cerebellum: organization and functional significance of the olivo-cerebellar system. Neuroscientist. 2007;13(6):616–25.

    Article  PubMed  CAS  Google Scholar 

  133. Riva D, Vago C, Usilla A, Treccani C, Pantaleoni C, DÆArrigo S, et al. The role of the cerebellum in higher cognitive and social functions in congenital and acquired diseases of developmental age. Biotechnologies vqgqtales: Numqro spqcial Cahiers Agricultures 2010;133.

  134. Granziera C, Schmahmann JD, Hadjikhani N, Meyer H, Meuli R, Wedeen V, et al. Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum in vivo. PLoS ONE. 2009;4(4):e5101.

    Article  PubMed  CAS  Google Scholar 

  135. Habas C. Functional imaging of the deep cerebellar nuclei: a review. Cerebellum 2009 Jun 10.

  136. Dias-Ferreira E, Sousa N, Costa RM. Frontocerebellar connectivity: climbing through the inferior olive. Frontiers in Neuroscience 2010;4.

  137. Mayor-Dubois C, Maeder P, Zesiger P, Roulet-Perez E. Visuo-motor and cognitive procedural learning in children with basal ganglia pathology. Neuropsychologia. 2010;48(7):2009–17.

    Article  PubMed  CAS  Google Scholar 

  138. Denckla MB, Reiss AL. Prefrontal–subcortical circuits in developmental disorders. In: Krasnegor NA, Lyon GR, Goldman-Rakic PS, editors. Development of the prefrontal cortex: evolution, neurobiology, and behavior. Baltimore: Brookes; 1997. p. 283–94.

    Google Scholar 

  139. Samango-Sprouse C. Frontal lobe development in childhood. The human frontal lobes: functions and disorders. 2007;576–93.

  140. Maia TV, Frank MJ. From reinforcement learning models to psychiatric and neurological disorders. Nat Neurosci. 2011;14(2):154–62.

    Article  PubMed  CAS  Google Scholar 

  141. Heilman KM, Valenstein E, Rothi LJG, Watson RT. Upper limb action—intentional and cognitive–apraxic motor disorders. Neurology in clinical practice. 5th ed. Philadelphia, PA: Elsevier; 2008. p. 121–32.

    Google Scholar 

  142. Heilman KM, Voeller KKS, Nadeau SE. A possible pathophysiologic substrate of attention deficit hyperactivity disorder. J Child Neurol. 1991;6(1 suppl):S76.

    PubMed  Google Scholar 

  143. Yin HH. The sensorimotor striatum is necessary for serial order learning. J Neurosci. 2010;30(44):14719–23.

    Article  PubMed  CAS  Google Scholar 

  144. Middleton FA. Fundamental and clinical evidence for basal ganglia influences on cognition. Mental and behavioral dysfunction in movement disorders. 2003;13–33.

  145. Morton JB, Munakata Y. Active versus latent representations: a neural network model of perseveration, dissociation, and decalage. Dev Psychobiol. 2002;40(3):255–65.

    Article  PubMed  Google Scholar 

  146. Chatham CH, Frank MJ, Munakata Y. Pupillometric and behavioral markers of a developmental shift in the temporal dynamics of cognitive control. Proc Natl Acad Sci. 2009;106(14):5529.

    Article  PubMed  CAS  Google Scholar 

  147. Lhermitte F, Pillon B, Serdaru M. Human autonomy and the frontal lobes. Part I: imitation and utilization behavior: a neuropsychological study of 75 patients. Ann Neurol. 1986;19(4):326–34.

    Article  PubMed  CAS  Google Scholar 

  148. Dehn M. Working memory and academy learning. Assessment and intervention. New Jersey: Wiley; 2008.

    Google Scholar 

  149. Logie RH, Engelkamp J, Dehn D, Rudkin S. Actions, mental actions, and working memory. Imagery, language and visuo-spatial thinking. 2001;161–83.

  150. Davidson MC, Amso D, Anderson LC, Diamond A. Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia. 2006;44(11):2037–78.

    Article  PubMed  Google Scholar 

  151. Diamond A. The early development of executive functions. Lifespan cognition: mechanisms of change. 2006;70–95.

  152. Finn AS, Sheridan MA, Kam CLH, Hinshaw S, D’Esposito M. Longitudinal evidence for functional specialization of the neural circuit supporting working memory in the human brain. J Neurosci. 2010;30(33):11062.

    Article  PubMed  CAS  Google Scholar 

  153. Munakata Y. Computational cognitive neuroscience of early memory development. Dev Rev. 2004;24(1):133–53.

    Article  Google Scholar 

  154. Gathercole SE. The development of memory. J Child Psychol Psychiatry. 1998;39(1):3–27.

    Article  PubMed  CAS  Google Scholar 

  155. Sobel N, Prabhakaran V, Hartley CA, Desmond JE, Zhao Z, Glover GH, et al. Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci. 1998;18(21):8990–9001.

    PubMed  CAS  Google Scholar 

  156. Zatorre RJ, Jones-Gotman M, Rouby C. Neural mechanisms involved in odor pleasantness and intensity judgments. Neuroreport. 2000;11(12):2711–6.

    Article  PubMed  CAS  Google Scholar 

  157. Parsons LM, Fox PT. Sensory and cognitive functions. In: Schmahmann J, editor. The cerebellum and cognition. San Diego: Academic; 1997. p. 255–72.

    Google Scholar 

  158. Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64(2):81–8.

    Article  PubMed  Google Scholar 

  159. Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46(7):831–44.

    Article  PubMed  Google Scholar 

  160. Imazu S, Sugio T, Tanaka S, Inui T. Differences between actual and imagined usage of chopsticks: an fMRI study. Cortex. 2007;43(3):301–7.

    Article  PubMed  Google Scholar 

  161. Hirano T, Watanabe D, Kawaguchi SY, Pastan I, Nakanishi S. Roles of inhibitory interneurons in the cerebellar cortex. Ann NY Acad Sci. 2002;978:405–12.

    Article  PubMed  CAS  Google Scholar 

  162. Jorntell H, Bengtsson F, Schonewille M, De Zeeuw CI. Cerebellar molecular layer interneurons—computational properties and roles in learning. Trends Neurosci. 2010;33(11):524–32.

    Article  PubMed  CAS  Google Scholar 

  163. Oldfield CS, Marty A, Stell BM. Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states. Proc Natl Acad Sci USA. 2010;107(29):13153–8.

    Article  PubMed  CAS  Google Scholar 

  164. Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67.

    Article  PubMed  Google Scholar 

  165. Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 2004;16(3):367–78.

    Article  PubMed  Google Scholar 

  166. Rosinski A, Goldman M, Cameron O. A case of cerebellar psychopathology. Psychosomatics. 2010;51(2):171.

    Article  PubMed  Google Scholar 

  167. Emul M, Yilmaz I, Asik A, Oruc S, Ilgaz K, Guler O. Co-occurrence of psychiatric symptoms with cerebellar venous malformation: a case report. J Neuropsychiatry Clin Neurosci. 2010;22(4):451-d.

    Article  PubMed  Google Scholar 

  168. Bostan AC, Strick PL. The cerebellum and basal ganglia are interconnected. Neuropsychol Rev. 2010;20(3):261–70.

    Article  PubMed  Google Scholar 

  169. Frank MJ. Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw. 2006;19(8):1120–36.

    Article  PubMed  Google Scholar 

  170. Frank MJ, Samanta J, Moustafa AA, Sherman SJ. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science. 2007;318(5854):1309–12.

    Article  PubMed  CAS  Google Scholar 

  171. Dunn W. Sensory profile caregiver questionnaire. San Antonio, TX: Psychological Corporation; 1999.

    Google Scholar 

  172. Raab M, Johnson JG, Heekeren HR. Mind and motion: the bidirectional link between thought and action. Amsterdam: Elsevier; 2009.

    Google Scholar 

  173. Dewey J. The reflex arc in psychology. Psychol Rev. 1896;3(1896):357–70.

    Article  Google Scholar 

  174. Nip ISB, Green JR, Marx DB. The coemergence of cognition, language, and speech motor control in early development: a longitudinal correlation study. Journal of Communication Disorders 2010.

  175. Iverson JM. Developing language in a developing body: the relationship between motor development and language development. J Child Lang. 2010;37(02):229–61.

    Article  PubMed  Google Scholar 

  176. Creem-Regehr SH. Sensory–motor and cognitive functions of the human posterior parietal cortex involved in manual actions. Neurobiol Learn Mem. 2009;91(2):166–71.

    Article  PubMed  Google Scholar 

  177. Meredith MA, Clemo HR. Corticocortical connectivity subserving different forms of multisensory convergence. In: Kaiser J, Naumer MJ, editors. Multisensory object perception in the primate brain. New York: Springer; 2010. p. 7–20.

    Chapter  Google Scholar 

  178. Kolb B, Whishaw IQ. Fundamentals of human neuropsychology. New York: Worth; 2008.

    Google Scholar 

  179. Heilman KM, Rothi LJG. Apraxia. In: Heilman KM, Valenstein E, editors. Clinical neuropsychology. 4th ed. New York: Oxford University Press; 2003. p. 215–35.

    Google Scholar 

  180. Gowen E, Miall RC. The cerebellum and motor dysfunction in neuropsychiatric disorders. Cerebellum. 2007;6(3):268–79.

    Article  PubMed  CAS  Google Scholar 

  181. Cools R, Frank MJ, Gibbs SE, Miyakawa A, Jagust W, D’Esposito M. Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci. 2009;29(5):1538–43.

    Article  PubMed  CAS  Google Scholar 

  182. Voogd J, Schraa-Tam CKL, van der Geest JN, De Zeeuw CI. Visuomotor cerebellum in human and nonhuman primates. The Cerebellum 2010;1–19.

  183. Davis EE, Pitchford NJ, Limback E. The interrelation between cognitive and motor development in typically developing children aged 4–11 years is underpinned by visual processing and fine manual control. British Journal of Psychology 2011.

  184. Haber SN. Integrative networks across basal ganglia circuits. Handbook Of Behavioral Neuroscience. 2010;20:409–28.

    Article  Google Scholar 

  185. Yin HH, Ostlund SB, Balleine BW. Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur J Neurosci. 2008;28(8):1437–48.

    Article  PubMed  Google Scholar 

  186. Haber SN, Calzavara R. The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull. 2009;78(2–3):69–74.

    Article  PubMed  Google Scholar 

  187. Jog M, Aur D. A theoretical information processing-based approach to basal ganglia function. The basal ganglia IX. 2009;211–22.

  188. Aarts E, Roelofs A, Franke B, Rijpkema M, Fernandez G, Helmich RC, et al. Striatal dopamine mediates the interface between motivational and cognitive control in humans: evidence from genetic imaging. Neuropsychopharmacology. 2010;35(9):1943–51.

    Article  PubMed  CAS  Google Scholar 

  189. Beck SM, Locke HS, Savine AC, Jimura K, Braver TS. Primary and secondary rewards differentially modulate neural activity dynamics during working memory. PLoS ONE. 2010;5(2):e9251.

    Article  PubMed  CAS  Google Scholar 

  190. Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY. Reward processing in autism. Autism Res. 2010;3(2):53–67.

    PubMed  Google Scholar 

  191. Walker MF, Tian J, Shan X, Tamargo RJ, Ying H, Zee DS, et al. The cerebellar nodulus/uvula integrates otolith signals for the translational vestibulo-ocular reflex. PLoS ONE. 2010;5(11):e13981.

    Article  PubMed  CAS  Google Scholar 

  192. Blatt GJ, Soghomonian JJ, Yip J. Glutamic acid decarboxylase (GAD) as a biomarker of GABAergic activity in autism: impact on cerebellar circuitry and function. The Neurochemical Basis of Autism 2010;95–111.

  193. Su CT, Wu MY, Yang AL, Chen-Sea MJ, Hwang IS. Impairment of stance control in children with sensory modulation disorder. Am J Occup Ther. 2010;64(3):443.

    Article  PubMed  Google Scholar 

  194. Mackie S, Shaw P, Lenroot R, Pierson R, Greenstein DK, Nugent III TF, et al. Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am J Psychiatry. 2007;164(4):647–55.

    Article  PubMed  Google Scholar 

  195. Fawcett AJ, Nicolson RI. Dyslexia, learning, and pedagogical neuroscience. Dev Med Child Neurol. 2007;49(4):306–11.

    Article  PubMed  Google Scholar 

  196. Stoodley CJ, Fawcett AJ, Nicolson RI, Stein JF. Impaired balancing ability in dyslexic children. Exp Brain Res. 2005;167(3):370–80.

    Article  PubMed  Google Scholar 

  197. Nicolson RI, Fawcett AJ, Brookes RL, Needle J. Procedural learning and dyslexia. Dyslexia. 2010;16(3):194–212.

    Article  PubMed  CAS  Google Scholar 

  198. Lonnemann J. Relations between balancing and arithmetic skills in children—evidence of cerebellar involvement? Journal of Neurolinguistics 2011.

  199. Haruno M, Wolpert DM, Kawato M. Multiple paired forward-inverse models for human motor learning and control. Advances in Neural Information Processing Systems 1999;31–7.

  200. Denckla MB. Measurement of executive function. In: Lyon GR, editor. Frames of reference for the assessment of learning disabilities: new views on measurement issues. Baltimore: Brookes; 1994. p. 117–42.

    Google Scholar 

  201. Butz M, Timmermann L, Gross J, Pollok B, Dirks M, Hefter H, et al. Oscillatory coupling in writing and writer’s cramp. J Physiol Paris. 2006;99(1):14–20.

    Article  PubMed  Google Scholar 

  202. Soteropoulos DS, Baker SN. Cortico-cerebellar coherence during a precision grip task in the monkey. J Neurophysiol. 2006;95(2):1194.

    Article  PubMed  Google Scholar 

  203. Taub AH, Mintz M. Amygdala conditioning modulates sensory input to the cerebellum. Neurobiology of Learning and Memory 2010.

  204. Koziol LF, Budding DE, Chidekel D. Adaptation, expertise, and giftedness: towards an understanding of cortical, subcortical, and cerebellar network contributions. The Cerebellum 2010;1–31.

  205. Ansari D. Neurocognitive approaches to developmental disorders of numerical and mathematical cognition: the perils of neglecting the role of development. Learning and Individual Differences 2009.

  206. Lebel C, Rasmussen C, Wyper K, Andrew G, Beaulieu C. Brain microstructure is related to math ability in children with fetal alcohol spectrum disorder. Alcohol Clin Exp Res. 2010;34(2):354–63.

    Article  PubMed  Google Scholar 

  207. Geary DC. Mathematical disabilities: reflections on cognitive, neuropsychological, and genetic components. Learn Individ Differ. 2010;20(2):130–3.

    Article  PubMed  Google Scholar 

  208. Gabriel A, Maillart C, Guillaume M, Meulemans T. Is there a generalized procedural deficit in children with specific language impairment? 6th International Conference on Language Acquisition (CIAL); Barcelona 2010.

  209. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the cortico–striatal and cortico–cerebellar systems to motor skill learning. Neuropsychologia. 2003;41(3):252–62.

    Article  PubMed  Google Scholar 

  210. Green D, Charman T, Pickles A, Chandler S, Loucas T, Simonoff E, et al. Impairment in movement skills of children with autistic spectrum disorders. Dev Med Child Neurol. 2009;51(4):311–6.

    Article  PubMed  Google Scholar 

  211. Zwicker JG, Missiuna C, Harris SR, Boyd LA. Brain activation of children with developmental coordination disorder is different than peers. Pediatrics. 2010;126(3):e678.

    Article  PubMed  Google Scholar 

  212. Gillig PM, Sanders RD. Psychiatry, neurology, and the role of the cerebellum. Psychiatry (Edgmont (Pa: Township)). 2010;7(9):38–43.

    Google Scholar 

  213. Ahlfors CE. Predicting bilirubin neurotoxicity in jaundiced newborns. Curr Opin Pediatr. 2010;22(2):129.

    Article  PubMed  Google Scholar 

  214. Amin SB, Prinzing D, Myers G. Hyperbilirubinemia and language delay in premature infants. Pediatrics. 2009;123(1):327–31.

    Article  PubMed  Google Scholar 

  215. Shapiro SM. Definition of the clinical spectrum of kernicterus and bilirubin-induced neurologic dysfunction (BIND). J Perinatol. 2004;25(1):54–9.

    Article  CAS  Google Scholar 

  216. Borsook D, Upadhyay J, Chudler EH, Becerra L. Review A key role of the basal ganglia in pain and analgesia—insights gained through human functional imaging. Mol Pain 2010;6(27):doi:10.1186/1744-8069-6-27.

  217. Adams-Chapman I. Insults to the developing brain and impact on neurodevelopmental outcome. J Commun Disord. 2009;42(4):256–62.

    Article  PubMed  Google Scholar 

  218. Back SA, Riddle A, McClure MM. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke. 2007;38(2 Suppl):724–30.

    Article  PubMed  Google Scholar 

  219. Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, et al. Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics. 2005;116(4):844–50.

    Article  PubMed  Google Scholar 

  220. Allen MC. Neurodevelopmental outcomes of preterm infants. Curr Opin Neurol. 2008;21(2):123.

    Article  PubMed  Google Scholar 

  221. Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, et al. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain. 2001;124(Pt 1):60–6.

    Article  PubMed  CAS  Google Scholar 

  222. Bodensteiner JB, Johnsen SD. Cerebellar injury in the extremely premature infant: newly recognized but relatively common outcome. J Child Neurol. 2005;20(2):139–42.

    Article  PubMed  Google Scholar 

  223. Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, et al. Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain. 2008;131(Pt 5):1344–51.

    PubMed  Google Scholar 

  224. Petrini JR, Dias T, McCormick MC, Massolo ML, Green NS, Escobar GJ. Increased risk of adverse neurological development for late preterm infants. J Pediatr. 2009;154(2):169–76.

    Article  PubMed  Google Scholar 

  225. Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R, et al. Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol. 2005;26(7):1659–67.

    PubMed  Google Scholar 

  226. Tiemeier H, Lenroot RK, Greenstein DK, Tran L, Pierson R, Giedd JN. Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage. 2010;49(1):63–70.

    Article  PubMed  Google Scholar 

  227. Weindling M. Insights into early brain development from modern brain imaging and outcome studies. Acta Pμdiatrica. 2010;99(7):961–6.

    Article  Google Scholar 

  228. Chu-Shore CJ, Kramer MA, Bianchi MT, Caviness VS, Cash SS. Network analysis: applications for the developing brain. Journal of Child Neurology 2011.

Download references

Conflicts of Interest

The authors have no conflicts of interest associated with this manuscript.

Author information

Authors and Affiliations

  1. Chicago, IL, USA

    Leonard F. Koziol

  2. Manhattan Beach, CA, USA

    Deborah Ely Budding

  3. Tarzana, CA, USA

    Dana Chidekel

Authors
  1. Leonard F. Koziol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deborah Ely Budding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dana Chidekel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deborah Ely Budding.

Additional information

The authors wish to acknowledge Jessica Chang for her research assistance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koziol, L.F., Budding, D.E. & Chidekel, D. Sensory Integration, Sensory Processing, and Sensory Modulation Disorders: Putative Functional Neuroanatomic Underpinnings. Cerebellum 10, 770–792 (2011). https://doi.org/10.1007/s12311-011-0288-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-011-0288-8

Keywords

Search

Navigation