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Current Sleep Medicine Reports

, Volume 5, Issue 3, pp 112–117 | Cite as

Behavioral States Modulate Sensory Processing in Early Development

  • James C. DooleyEmail author
  • Greta Sokoloff
  • Mark S. Blumberg
Sleep and Development (L Tarokh, Section Editor)
  • 19 Downloads
Part of the following topical collections:
  1. Topical Collection on Sleep and Development

Abstract

Purpose of Review

Sleep-wake states modulate cortical activity in adults. In infants, however, such modulation is less clear; indeed, early cortical activity comprises bursts of neural activity driven predominantly by peripheral sensory input. Consequently, in many studies of sensory development in rodents, sensory processing has been carefully investigated, but the modulatory role of behavioral state has typically been ignored.

Recent Findings

In the developing visual and somatosensory systems, it is now known that sleep and wake states modulate sensory processing. Further, in both systems, the nature of this modulation shifts rapidly during the second postnatal week, with subcortical nuclei changing how they gate sensory inputs.

Summary

The interactions among sleep and wake movements, sensory processing, and development are dynamic and complex. Now that established methods exist to record neural activity in unanesthetized infant animals, we can provide a more comprehensive understanding of how infant sleep-wake states interact with sensory-driven responses to promote developmental plasticity.

Keywords

Cortical development REM sleep Activity-dependent development Movement Visual system Somatosensory system 

Notes

Compliance with Ethical Standards

Conflict of Interest

James C. Dooley, Greta Sokoloff, and Mark S. Blumberg each declare no conflict of interest.

Human and Animal Rights Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol. 1970;2:216–39.CrossRefGoogle Scholar
  2. 2.
    Roffwarg HP, Muzio JN, Dement WC. Ontogenetic development of the human sleep-dream cycle. Science. 1966;152:604–19.CrossRefGoogle Scholar
  3. 3.
    Vanhatalo S, Kaila K. Development of neonatal EEG activity: from phenomenology to physiology. Seminars in fetal & neonatal medicine. 2006;11(6):471–8.CrossRefGoogle Scholar
  4. 4.
    Tsuchida TN, Wusthoff CJ, Shellhaas RA, Abend NS, Hahn CD, Sullivan JE, et al. American clinical neurophysiology society standardized EEG terminology and categorization for the description of continuous EEG monitoring in neonates: report of the American Clinical Neurophysiology Society critical care monitoring committee. Journal of clinical neurophysiology. 2013;30(2):161–73.CrossRefGoogle Scholar
  5. 5.
    Colonnese MT, Kaminska A, Minlebaev M, Milh M, Bloem B, Lescure S, et al. A conserved switch in sensory processing prepares developing neocortex for vision. Neuron. 2010;67(3):480–98.CrossRefGoogle Scholar
  6. 6.
    Seelke AMH, Blumberg MS. Developmental appearance and disappearance of cortical events and oscillations in infant rats. Brain Res. 2010;1324:34–42.CrossRefGoogle Scholar
  7. 7.
    Frank MG, Heller HC. Development of REM and slow wave sleep in the rat. Am J Physiol. 1997;272:R1792–R9.Google Scholar
  8. 8.
    Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature. 2004;432:758–61.CrossRefGoogle Scholar
  9. 9.
    Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex. 2007;17(7):1582–94.CrossRefGoogle Scholar
  10. 10.
    Clawson BC, Durkin J, Aton SJ. Form and function of sleep spindles across the lifespan. Neural Plast. 2016;6936381:1–16.CrossRefGoogle Scholar
  11. 11.
    Hanganu IL, Ben-Ari Y, Khazipov R. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci. 2006;26(25):6728–36.CrossRefGoogle Scholar
  12. 12.
    • Murata Y, Colonnese MT. An excitatory cortical feedback loop gates retinal wave transmission in rodent thalamus. eLife. 2016;5. Using the rat visual system, this paper documents the change in corticothalamic feedback responsible for the production of spindle bursts. Google Scholar
  13. 13.
    Chipaux M, Colonnese MT, Mauguen A, Fellous L, Mokhtari M, Lezcano O, et al. Auditory stimuli mimicking ambient sounds drive temporal “delta-brushes” in premature infants. PLoS One. 2013;8(11):e79028.CrossRefGoogle Scholar
  14. 14.
    An S, Kilb W, Luhmann HJ. Sensory-evoked and spontaneous gamma and spindle bursts in neonatal rat motor cortex. J Neurosci. 2014;34(33):10870–83.CrossRefGoogle Scholar
  15. 15.
    Tiriac A, Del Rio-Bermudez C, Blumberg MS. Self-generated movements with “unexpected” sensory consequences. Curr Biol. 2014;24(18):2136–41.CrossRefGoogle Scholar
  16. 16.
    Brockmann MD, Poschel B, Cichon N, Hanganu-Opatz IL. Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron. 2011;71(2):332–47.CrossRefGoogle Scholar
  17. 17.
    Yang JW, Hanganu-Opatz IL, Sun JJ, Luhmann HJ. Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci. 2009;29(28):9011–25.CrossRefGoogle Scholar
  18. 18.
    Mizuno H, Ikezoe K, Nakazawa S, Sato T, Kitamura K, Iwasato T. Patchwork-type spontaneous activity in neonatal barrel cortex layer 4 transmitted via thalamocortical projections. Cell Rep. 2018;22(1):123–35.CrossRefGoogle Scholar
  19. 19.
    Tolner EA, Sheikh A, Yukin AY, Kaila K, Kanold PO. Subplate neurons promote spindle bursts and thalamocortical patterning in the neonatal rat somatosensory cortex. J Neurosci. 2012;32(2):692–702.CrossRefGoogle Scholar
  20. 20.
    Colonnese MT, Phillips MA. Thalamocortical function in developing sensory circuits. Curr Opin Neurobiol. 2018;52:72–9.CrossRefGoogle Scholar
  21. 21.
    Huberman AD, Feller MB, Chapman B. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci. 2008;31:479–509.CrossRefGoogle Scholar
  22. 22.
    Tiriac A, Smith BE, Feller MB. Light prior to eye opening promotes retinal waves and eye-specific segregation. Neuron. 2018;100(5):1059–65.e4.CrossRefGoogle Scholar
  23. 23.
    Ackman JB, Burbridge TJ, Crair MC. Retinal waves coordinate patterned activity throughout the developing visual system. Nature. 2012;490(7419):219–25.CrossRefGoogle Scholar
  24. 24.
    • Mukherjee D, Yonk AJ, Sokoloff G, Blumberg MS. Wakefulness suppresses retinal wave-related neural activity in visual cortex. J Neurophysiol. 2017;118(2):1190–7 Describes the inhibition of sensory responses in V1 during active wake through P12 in rats. CrossRefGoogle Scholar
  25. 25.
    •• Murata Y, Colonnese MT. Thalamus controls development and expression of arousal states in visual cortex. J Neurosci. 2018;38(41):8772–86 Describes inhibition of sensory responses in V1 and dLGN during active wake at P11 and before, but not after P13. CrossRefGoogle Scholar
  26. 26.
    Dipoppa M, Ranson A, Krumin M, Pachitariu M, Carandini M, Harris KD. Vision and locomotion shape the interactions between neuron types in mouse visual cortex. Neuron. 2018;98(3):602–15.e8.CrossRefGoogle Scholar
  27. 27.
    Niell CM, Stryker MP. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron. 2010;65(4):472–9.CrossRefGoogle Scholar
  28. 28.
    Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP, Nicoll RA, et al. A cortical circuit for gain control by behavioral state. Cell. 2014;156(6):1139–52.CrossRefGoogle Scholar
  29. 29.
    Small WS. Notes on the psychic development of the young white rat. Am J Psychol. 1899;11(1):80–100.CrossRefGoogle Scholar
  30. 30.
    Alberts JR. Huddling by rat pups: ontogeny of individual and group behavior. Dev Psychobiol. 2007;49(1):22–32.CrossRefGoogle Scholar
  31. 31.
    Westneat MW, Hall WG. Ontogeny of feeding motor patterns in infant rats: AN electromyographic analysis of suckling and chewing. Behav Neurosci. 1992;106:539–54.CrossRefGoogle Scholar
  32. 32.
    Shriner AM, Drever FR, Metz GA. The development of skilled walking in the rat. Behav Brain Res. 2009;205(2):426–35.CrossRefGoogle Scholar
  33. 33.
    Kreider JC, Blumberg MS. Mesopontine contribution to the expression of active ‘twitch’ sleep in decerebrate week-old rats. Brain Res. 2000;872:149–59.CrossRefGoogle Scholar
  34. 34.
    Young NA, Vuong J, Teskey GC. Development of motor maps in rats and their modulation by experience. J Neurophysiol. 2012;108(5):1309–17.CrossRefGoogle Scholar
  35. 35.
    Martin JH. The corticospinal system: from development to motor control. Neuroscientist. 2005;11(2):161–73.CrossRefGoogle Scholar
  36. 36.
    Chakrabarty S, Martin JH. Postnatal development of the motor representation in primary motor cortex. J Neurophysiol. 2000;84:2582–94.CrossRefGoogle Scholar
  37. 37.
    Del Rio-Bermudez C, Sokoloff G, Blumberg MS. Sensorimotor processing in the newborn rat red nucleus during active sleep. J Neurosci. 2015;35(21):8322–32.CrossRefGoogle Scholar
  38. 38.
    •• Dooley JC, Blumberg MS. Developmental ‘awakening’ of primary motor cortex to the sensory consequences of movement. eLife. 2018;7:e41841. Documents change in the processing of reafference from wake movements in the ECN. Reafference from wake movements is inhibited in the ECN, and thus does not reach sensorimotor cortex, at P10, but this inhibition is lifted at P11. Google Scholar
  39. 39.
    Blumberg MS, Coleman CM, Gerth AI, McMurray B. Spatiotemporal structure of REM sleep twitching reveals developmental origins of motor synergies. Curr Biol. 2013;23(21):2100–9.CrossRefGoogle Scholar
  40. 40.
    • Tiriac AB, Blumberg MS. Gating of reafference in the external cuneate nucleus during wake movements but not sleep-related twitches. eLife. 2016;5:e18749. Describes the role of the ECN in inhibiting reafference from wake movements while permitting reafference from twitches to activate sensorimotor cortex. Google Scholar
  41. 41.
    Boivie J, Boman K. Termination of a separate (proprioceptive?) cuneothalamic tract from external cuneate nucleus in monkey. Brain Res. 1981;224(2):235–46.CrossRefGoogle Scholar
  42. 42.
    Campbell SK, Parker TD, Welker W. Somatotopic organization of the external cuneate nucleus in albino rats. Brain Res. 1974;77(1):1–23.CrossRefGoogle Scholar
  43. 43.
    Failor S, Chapman B, Cheng HJ. Retinal waves regulate afferent terminal targeting in the early visual pathway. Proc Natl Acad Sci U S A. 2015;112(22):E2957–66.CrossRefGoogle Scholar
  44. 44.
    Davis ZW, Chapman B, Cheng HJ. Increasing spontaneous retinal activity before eye opening accelerates the development of geniculate receptive fields. J Neurosci. 2015;35(43):14612–23.CrossRefGoogle Scholar
  45. 45.
    Khateb M, Schiller J, Schiller Y. Feedforward motor information enhances somatosensory responses and sharpens angular tuning of rat S1 barrel cortex neurons. eLife. 2017;6:e21843.Google Scholar
  46. 46.
    Ferezou I, Bolea S, Petersen CC. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron. 2006;50(4):617–29.CrossRefGoogle Scholar
  47. 47.
    Blumberg MS. Developing sensorimotor systems in our sleep. Curr Dir Psychol Sci. 2015;24(1):32–7.CrossRefGoogle Scholar
  48. 48.
    Eggermann E, Kremer Y, Crochet S, Petersen CCH. Cholinergic signals in mouse barrel cortex during active whisker sensing. Cell Rep. 2014;9(5):1654–60.CrossRefGoogle Scholar
  49. 49.
    Aston-Jones G, Cohen JD. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci. 2005;28:403–50.CrossRefGoogle Scholar
  50. 50.
    Guzman-Marin R, Alam MN, Szymusiak R, Drucker-Colin R, Gong H, McGinty D. Discharge modulation of rat dorsal raphe neurons during sleep and waking: effects of preoptic/basal forebrain warming. Brain Res. 2000;875(1–2):23–34.CrossRefGoogle Scholar
  51. 51.
    Kiss J, Patel AJ. Development of the cholinergic fibres innervating the cerebral cortex of the rat. Int J Dev Neurosci. 1992;10(2):153–70.CrossRefGoogle Scholar
  52. 52.
    Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HB. Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol. 1988;269(1):58–72.CrossRefGoogle Scholar
  53. 53.
    Tarazi FI, Baldessarini RJ. Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci. 2000;18(1):29–37.CrossRefGoogle Scholar
  54. 54.
    Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE. The origin of spontaneous activity in the developing auditory system. Nature. 2007;450(7166):50–5.CrossRefGoogle Scholar
  55. 55.
    Wang HC, Bergles DE. Spontaneous activity in the developing auditory system. Cell Tissue Res. 2015;361(1):65–75.CrossRefGoogle Scholar
  56. 56.
    • Wess JM, Isaiah A, Watkins PV, Kanold PO. Subplate neurons are the first cortical neurons to respond to sensory stimuli. Proc Natl Acad Sci U S A. 2017;114(47):12602–7 Using the ferret auditory system, this paper to shows that subplate neurons are the first cortical neurons to respond to auditory stimuli.CrossRefGoogle Scholar
  57. 57.
    Kandler K, Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol. 1993;328(2):161–84.CrossRefGoogle Scholar
  58. 58.
    Blumberg MS, Seelke AMH, Lowen SB, Karlsson KÆ. Dynamics of sleep-wake cyclicity in developing rats. Proc Natl Acad Sci. 2005;102(41):14860–4.CrossRefGoogle Scholar
  59. 59.
    Mashour GA. Top-down mechanisms of anesthetic-induced unconsciousness. Front Syst Neurosci. 2014;8(115).Google Scholar
  60. 60.
    Blumberg MS, Sokoloff G, Tiriac A, Del Rio-Bermudez C. A valuable and promising method for recording brain activity in behaving newborn rodents. Dev Psychobiol. 2015;57(4):506–17.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • James C. Dooley
    • 1
    • 2
    Email author
  • Greta Sokoloff
    • 1
    • 2
    • 3
  • Mark S. Blumberg
    • 1
    • 2
    • 3
    • 4
    • 5
  1. 1.Department of Psychological & Brain SciencesUniversity of IowaIowa CityUSA
  2. 2.DeLTA CenterUniversity of IowaIowa CityUSA
  3. 3.Iowa Neuroscience InstituteUniversity of IowaIowa CityUSA
  4. 4.Interdisciplinary Graduate Program in NeuroscienceUniversity of IowaIowa CityUSA
  5. 5.Department of BiologyUniversity of IowaIowa CityUSA

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