Advertisement

Experimental Brain Research

, Volume 153, Issue 4, pp 543–549 | Cite as

Functional organization of lemniscal and nonlemniscal auditory thalamus

Review

Abstract

Thalamic nuclei of the mammalian auditory system exhibit remarkable parallelism in their anatomical pathways and the patterns of synaptic signalling. This has led to the theory that lemniscal, or core thalamocortical projection, carries tonotopically organized and auditory specific information whereas the nonlemniscal thalamocortical pathway forms part of an integrative system that plays an important role in polysensory integration, temporal pattern recognition, and certain forms of learning. Recent experimental evidence derived from molecular, cellular and behavioural studies indeed supports the conjecture that lemniscal and nonlemniscal pathways are involved in distinctive auditory functions.

Keywords

Auditory Thalamocortical pathways Lemniscal projections Nonlemniscal projections Review 

References

  1. Ahissar E, Sosnik R, Haidarliu S (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406:302–306CrossRefPubMedGoogle Scholar
  2. Aitkin LM, Prain SM (1974) Medial geniculate body: unit responses in the awake cat. J Neurophysiol 37:512–521PubMedGoogle Scholar
  3. Andersen RA, Knight PL, Merzenich MM (1980) The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J Comp Neurol 194:663–701PubMedGoogle Scholar
  4. Bartlett EL, Smith PH (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol 81:1999–2016PubMedGoogle Scholar
  5. Bordi F, LeDoux JE (1994a) Response properties of single units in areas of rat auditory thalamus that project to the amygdala. I. Acoustic discharge patterns and frequency receptive fields. Exp Brain Res 98:261–274PubMedGoogle Scholar
  6. Bordi F, LeDoux JE (1994b) Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp Brain Res 98:275–286PubMedGoogle Scholar
  7. Brecht M, Sakmann B (2002) Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol 538:495–515CrossRefPubMedGoogle Scholar
  8. Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364PubMedGoogle Scholar
  9. Calford MB, Aitkin LM (1983) Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365–2380PubMedGoogle Scholar
  10. Carr C (2002) Sounds, signals and space maps. Nature 415:29–31CrossRefPubMedGoogle Scholar
  11. Clarey JC, Irvine DR (1990) The anterior ectosylvian sulcal auditory field in the cat. II. A horseradish peroxidase study of its thalamic and cortical connections. J Comp Neurol 301:304–324PubMedGoogle Scholar
  12. Clugnet MC, LeDoux JE (1990) Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J Neurosci 10:2818–2824PubMedGoogle Scholar
  13. Collins DR, Paré D (2000) Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS+ and CS. Learn Mem 7:97–103CrossRefPubMedGoogle Scholar
  14. Cruikshank SJ, Killackey HP, Metherate R (2001) Parvalbumin and calbindin are differentially distributed within primary and secondary subregions of the mouse auditory forebrain. Neuroscience 105:553–569CrossRefPubMedGoogle Scholar
  15. Deschenes M, Bourassa J, Pinault D (1994) Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res 664:215–219PubMedGoogle Scholar
  16. Deschenes M, Veinante P, Zhang ZW (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Res Brain Res Rev 28:286–308PubMedGoogle Scholar
  17. Destexhe A, Neubig M, Ulrich D, Huguenard J (1998) Dendritic low-threshold calcium currents in thalamic relay cells. J Neurosci 18:3574–3588PubMedGoogle Scholar
  18. Diamond ME (2000) Neurobiology. Parallel sensing. Nature 406:245–247CrossRefPubMedGoogle Scholar
  19. Doron NN, Ledoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412:383–409Google Scholar
  20. Doron NN, Ledoux JE (2000) Cells in the posterior thalamus project to both amygdala and temporal cortex: a quantitative retrograde double-labeling study in the rat. J Comp Neurol 425:257–274CrossRefPubMedGoogle Scholar
  21. Druga R, Syka J (1993) NADPH-diaphorase activity in the central auditory structures of the rat. Neuroreport 4:999–1002PubMedGoogle Scholar
  22. Duncan GE, Henson OW (1994) Brain activity patterns in flying, echolocating bats (Pteronotus parnellii): assessment by high resolution autoradiographic imaging with [3H]2-deoxyglucose. Neuroscience 59:1051–1070CrossRefPubMedGoogle Scholar
  23. Duvel AD, Smith DM, Talk A, Gabriel M (2001) Medial geniculate, amygdalar and cingulate cortical training-induced neuronal activity during discriminative avoidance learning in rabbits with auditory cortical lesions. J Neurosci 21:3271–3281PubMedGoogle Scholar
  24. Edeline JM (1999) Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog Neurobiol 57:165–224CrossRefPubMedGoogle Scholar
  25. Edeline JM, Weinberger NM (1992) Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behav Neurosci 106:81–105PubMedGoogle Scholar
  26. Edeline JM, Manunta Y, Nodal FR, Bajo VM (1999) Do auditory responses recorded from awake animals reflect the anatomical parcellation of the auditory thalamus? Hear Res 131:135–152CrossRefPubMedGoogle Scholar
  27. Edeline JM, Manunta Y, Hennevin E (2000) Auditory thalamus neurons during sleep: changes in frequency selectivity, threshold, and receptive field size. J Neurophysiol 84:934–952PubMedGoogle Scholar
  28. Fitzpatrick D, Diamond IT, Raczkowski D (1989) Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J Comp Neurol 288:647–675PubMedGoogle Scholar
  29. Fitzpatrick DC, Olsen JF, Suga N (1998) Connections among functional areas in the mustached bat auditory cortex. J Comp Neurol 391:366–396CrossRefPubMedGoogle Scholar
  30. Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc Natl Acad Sci USA 97:8081–8086CrossRefPubMedGoogle Scholar
  31. Gonzalez-Lima F, Cada A (1994) Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience 63:559–578CrossRefPubMedGoogle Scholar
  32. Graybiel AM (1972) Some ascending connections of the pulvinar and nucleus lateralis posterior of the thalamus in the cat. Brain Res 44:99–125CrossRefPubMedGoogle Scholar
  33. He J (2001) On and off pathways segregated at the auditory thalamus of the guinea pig. J Neurosci 21:8672–8679PubMedGoogle Scholar
  34. He J, Hashikawa T (1998) Connections of the dorsal zone of cat auditory cortex. J Comp Neurol 400:334–348CrossRefPubMedGoogle Scholar
  35. He J, Hu B (2002) Differential distribution of burst and single-spike responses in auditory thalamus. J Neurophysiol 88:2152–2156PubMedGoogle Scholar
  36. Hu B (1995) Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. J Physiol 483:167–182PubMedGoogle Scholar
  37. Hu B, Steriade M, Deschenes M (1989) The cellular mechanism of thalamic ponto-geniculo-occipital waves. Neuroscience 31:25–35CrossRefPubMedGoogle Scholar
  38. Hu B, Senatorov V, Mooney D (1994) Lemniscal and non-lemniscal synaptic transmission in rat auditory thalamus. J Physiol 479:217–231PubMedGoogle Scholar
  39. Huang YY, Martin KC, Kandel ER (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci 20:6317–6325PubMedGoogle Scholar
  40. Hughes SW, Cope DW, Toth TI, Williams SR, Crunelli V (1999) All thalamocortical neurones possess a T-type Ca2+ 'window' current that enables the expression of bistability-mediated activities. J Physiol 517:805–815PubMedGoogle Scholar
  41. Imig TJ, Morel A (1983) Organization of the thalamocortical auditory system in the cat. Annu Rev Neurosci 6:95–120CrossRefPubMedGoogle Scholar
  42. Inglis WL, Winn P (1995) The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol 47:1–29PubMedGoogle Scholar
  43. Iwata K, Kenshalo DR, Jr., Dubner R, Nahin RL (1992) Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J Comp Neurol 321:404–420PubMedGoogle Scholar
  44. Jahnsen H, Llinas R (1984a) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205–226PubMedGoogle Scholar
  45. Jahnsen H, Llinas R (1984b) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227–247PubMedGoogle Scholar
  46. Jones EG (1985) The thalamus. Plenum Press, New YorkGoogle Scholar
  47. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601Google Scholar
  48. Kakei S, Na J, Shinoda Y (2001) Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J Comp Neurol 437:170–185Google Scholar
  49. Kelly JB (1973) The effects of insular and temporal lesions in cats on two types of auditory pattern discrimination. Brain Res 62:71–87CrossRefPubMedGoogle Scholar
  50. Knudsen EI, Zheng W, DeBello WM (2000) Traces of learning in the auditory localization pathway. Proc Natl Acad Sci USA 97:11815–11820CrossRefPubMedGoogle Scholar
  51. Komura Y, Tamura R, Uwano T, Nishijo H, Kaga K, Ono T (2001) Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature 412:546–549CrossRefPubMedGoogle Scholar
  52. Kraus N, McGee T (1995) The middle latency response generating system. Electroencephalogr Clin Neurophysiol Suppl 44:93–101PubMedGoogle Scholar
  53. Kraus N, McGee T, Littman T, Nicol T, King C (1994) Nonprimary auditory thalamic representation of acoustic change. J Neurophysiol 72:1270–1277PubMedGoogle Scholar
  54. Kraus N, McGee T, Carrell TD, Sharma A (1995) Neurophysiologic bases of speech discrimination. Ear Hear 16:19–37PubMedGoogle Scholar
  55. Layton BS, Toga AW, Horenstein S, Davenport DG (1979) Temporal pattern discrimination survives simultaneous bilateral ablation of suprasylvian cortex but not sequential bilateral ablation of insular-temporal cortex in the cat. Brain Res 173:337–340CrossRefPubMedGoogle Scholar
  56. LeDoux J (1996) Emotional networks and motor control: a fearful view. Prog Brain Res 107:437–446PubMedGoogle Scholar
  57. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184PubMedGoogle Scholar
  58. Ledoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123–146Google Scholar
  59. Lennartz RC, Weinberger NM (1992) Frequency selectivity is related to temporal processing in parallel thalamocortical auditory pathways. Brain Res 583:81–92PubMedGoogle Scholar
  60. Levey AI, Hallanger AE, Wainer BH (1987) Choline acetyltransferase immunoreactivity in the rat thalamus. J Comp Neurol 257:317–332PubMedGoogle Scholar
  61. Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38–43PubMedGoogle Scholar
  62. Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301–304Google Scholar
  63. Maren S (1999) Long-term potentiation in the amygdala: a mechanism for emotional learning and memory. Trends Neurosci 22:561–567PubMedGoogle Scholar
  64. Markram H, Sakmann B (1994) Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc Natl Acad Sci USA 91:5207–5211PubMedGoogle Scholar
  65. Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM–Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976PubMedGoogle Scholar
  66. McKernan MG, Shinnick-Gallagher P (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390:607–611Google Scholar
  67. Mellor J, Nicoll RA, Schmitz D (2002) Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295:143–147CrossRefPubMedGoogle Scholar
  68. Merabet L, Desautels A, Minville K, Casanova C (1998) Motion integration in a thalamic visual nucleus. Nature 396:265–268PubMedGoogle Scholar
  69. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1–Ch6). Neuroscience 10:1185–1201PubMedGoogle Scholar
  70. Miller LM, Schreiner CE (2000) Stimulus-based state control in the thalamocortical system. J Neurosci 20:7011–7016PubMedGoogle Scholar
  71. Miller LM, Escabi MA, Read HL, Schreiner CE (2001a) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151–160PubMedGoogle Scholar
  72. Miller LM, Escabi MA, Schreiner CE (2001b) Feature selectivity and interneuronal cooperation in the thalamocortical system. J Neurosci 21:8136–8144PubMedGoogle Scholar
  73. Mooney DM (2001) Cholinergic control of sensory synaptic transmission in primary and nonprimary auditory thalamus of rat. Department of Cellular and Molecular Medicine, Faculty of Medicine, University of Ottawa, Ottawa, p 172Google Scholar
  74. Mooney DM, Hu B (2002) Induction of long-term potentiation in the thalamoamygdala pathway by burst stimulation. Program no. 659.2 of 2002 Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington DC. Available online http://sfn.scholarone.com/itin2002/index.htmlGoogle Scholar
  75. Mooney DM, Hu B, Senatorov VV (1995) Muscarine induces an anomalous inhibition of synaptic transmission in rat auditory thalamic neurons in vitro. J Pharmacol Exp Ther 275:838–844PubMedGoogle Scholar
  76. Moosmang S, Biel M, Hofmann F, Ludwig A (1999) Differential distribution of four hyperpolarization-activated cation channels in mouse brain. Biol Chem 380:975–980PubMedGoogle Scholar
  77. Neff WD, Casseday JH, Cranford JL (1972) The medial geniculate body and associated thalamic cell groups: behavioral studies. Brain Behav Evol 6:302–310PubMedGoogle Scholar
  78. Ojima H (1994) Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb Cortex 4:646–663PubMedGoogle Scholar
  79. Olsen JF, Suga N (1991a) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J Neurophysiol 65:1254–1274PubMedGoogle Scholar
  80. Olsen JF, Suga N (1991b) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information. J Neurophysiol 65:1275–1296PubMedGoogle Scholar
  81. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 65:113–136CrossRefPubMedGoogle Scholar
  82. Raczkowski D, Diamond IT, Winer J (1976) Organization of thalamocortical auditory system in the cat studied with horseradish peroxidase. Brain Res 101:345–354CrossRefPubMedGoogle Scholar
  83. Rouiller EM, Wan XS, Moret V, Liang F (1992) Mapping of c-fos expression elicited by pure tones stimulation in the auditory pathways of the rat, with emphasis on the cochlear nucleus. Neurosci Lett 144:19–24CrossRefPubMedGoogle Scholar
  84. Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20:5264–5275PubMedGoogle Scholar
  85. Semba K, Reiner PB, Fibiger HC (1990) Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38:643–654PubMedGoogle Scholar
  86. Senatorov VV, Hu B (1997) Differential Na+–K+-ATPase activity in rat lemniscal and non-lemniscal auditory thalami. J Physiol 502:387–395PubMedGoogle Scholar
  87. Senatorov V, Hu B (2000) Differential neuronal distribution of inward rectifying conductances in rat auditory thalamus. Soc Neurosci Abstr 26, Program no. 637.2Google Scholar
  88. Senatorov VV, Mooney D, Hu B (1997) The electrogenic effects of Na+–K+-ATPase in rat auditory thalamus. J Physiol 502:375–385PubMedGoogle Scholar
  89. Sherman SM (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122–126CrossRefPubMedGoogle Scholar
  90. Shinonaga Y, Takada M, Mizuno N (1994) Direct projections from the non-laminated divisions of the medial geniculate nucleus to the temporal polar cortex and amygdala in the cat. J Comp Neurol 340:405–426PubMedGoogle Scholar
  91. Steriade M (1990) Cholinergic control of thalamic function [in French]. Arch Int Physiol Biochim 98:A11–A46PubMedGoogle Scholar
  92. Steriade M (1996) Arousal: revisiting the reticular activating system. Science 272:225–226Google Scholar
  93. Suga N (1990) Biosonar and neural computation in bats. Sci Am 262:60–68PubMedGoogle Scholar
  94. Suga N, Gao E, Zhang Y, Ma X, Olsen JF (2000) The corticofugal system for hearing: recent progress. Proc Natl Acad Sci USA 97:11807–11814CrossRefPubMedGoogle Scholar
  95. Tennigkeit F, Puil E, Schwarz DW (1997) Firing modes and membrane properties in lemniscal auditory thalamus. Acta Otolaryngol 117:254–257PubMedGoogle Scholar
  96. Weinberger NM (1995) Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annu Rev Neurosci 18:129–158PubMedGoogle Scholar
  97. Weinberger NM (1998) Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol Learn Mem 70:226–251CrossRefPubMedGoogle Scholar
  98. Weinberger NM, Bakin JS (1998) Learning-induced physiological memory in adult primary auditory cortex: receptive fields plasticity, model, and mechanisms. Audiol Neurootol 3:145–167Google Scholar
  99. Williams SR, Stuart GJ (2000) Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J Neurosci 20:1307–1317PubMedGoogle Scholar
  100. Williams JA, Comisarow J, Day J, Fibiger HC, Reiner PB (1994) State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis. J Neurosci 14:5236–5242PubMedGoogle Scholar
  101. Winer J (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper, AN, Fay RR (eds) The mammalian auditory pathway. Springer-Verlag, Berlin Heidelberg New York, pp 222–409Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Clinical Neurosciences and Neuroscience Research GroupUniversity of CalgaryCalgaryCanada

Personalised recommendations