Advertisement

Experimental Brain Research

, Volume 184, Issue 2, pp 179–191 | Cite as

Laminar differences in the response properties of cells in the primary auditory cortex

  • M. N. WallaceEmail author
  • A. R. Palmer
Research Article

Abstract

In visual and somatosensory cortex there are important functional differences between layers. Although it is difficult to identify laminar borders in the primary auditory cortex (AI) laminar differences in functional processing are still present. We have used electrodes inserted orthogonal to the cortical surface to compare the response properties of cells in all six layers of AI in anaesthetised guinea pigs. Cells were stimulated with short tone pips and two conspecific vocalizations. When frequency response areas were measured for 248 units the tuning bandwidth was broader for units in the deep layers. The mean Q 10 value for tuning in layers IV–VI was significantly smaller (Mann–Whitney test P < 0.001) than for layers I–III. When response latencies were measured, the shortest latencies were found in layer V and the mean latency in this layer was shorter than in any of the more superficial layers (I–IV) when compared with a Tukey analysis of variance (P < 0.005). There were also laminar differences in the best threshold with layer V having the highest mean value. The mean best threshold for layer V (32.7 dB SPL) was significantly different from the means for layers II (25.5 dB SPL) and III (26.3 dB SPL). The responses to two vocalizations also varied between layers: the response to the first phrase of a chutter was smaller and about 10 ms later in the deep layers than in layers II and III. By contrast, the response to an example of whistle was stronger in the deep layers. These results are consistent with a model of AI that involves separate inputs to different layers and descending outputs from layers V/VI (to thalamus and brainstem) that are different from the output from layers II/III (to ipsilateral cortex).

Keywords

Cortical layers Frequency response areas First spike latency Vocalizations Best threshold Tuning bandwidth 

Notes

Acknowledgments

We wish to thank Prof. J. Syka for providing us with digitized recordings of the guinea pig chutter and whistle. We also thank Dr. TM Shackleton for preparing our in-house software to present stimuli and capture the responses, Dr. JWH Schnupp for use of Brainware in multielectrode recording and Dr. KT Nakamoto for commenting on the manuscript.

References

  1. Abeles M, Goldstein MH Jr (1970) Functional architecture in cat primary auditory cortex: columnar organization and organization according to depth. J Neurophysiol 33:172–187PubMedGoogle Scholar
  2. Anderson LA, Wallace MN, Palmer AR (2007) Identification of subdivisions in the medial geniculate body of the guinea pig. Hear Res 228:156–167PubMedCrossRefGoogle Scholar
  3. Arnott RH, Wallace MN, Shackleton TM, Palmer AR (2004) Onset neurons in the anteroventral cochlear nucleus project to the dorsal cochlear nucleus. J Assoc Res Otolaryngol 5:153–170PubMedGoogle Scholar
  4. Atencio CA, Schreiner CE (2005) Topographical laminar distribution of receptive field parameters in the primary auditory cortex of the cat. Assoc Res Otolaryngol Abstr 28:353Google Scholar
  5. Berryman JC (1976) Guinea-pig vocalizations: their structure, causation and function. Z Tierpsychol 41:80–106PubMedGoogle Scholar
  6. Bieser A (1998) Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys. Exp Brain Res 122:139–148PubMedCrossRefGoogle Scholar
  7. Bullock D, Palmer AR, Rees A (1988) A compact and easy to use tungsten in glass microelectrode manufacturing workstation. Med Biol Eng Comput 26:669–672PubMedCrossRefGoogle Scholar
  8. Coomes DL, Schofield RM, Schofield BR (2005) Unilateral and bilateral projections from cortical cells to the inferior colliculus in guinea pigs. Brain Res 1042:62–72PubMedCrossRefGoogle Scholar
  9. Creutzfeldt OD, Hellweg F-C, Schreiner CE (1980) Thalamocortical transformation of responses to complex auditory stimuli. Exp Brain Res 39:87–104PubMedCrossRefGoogle Scholar
  10. Douglas RJ, Martin KAC (2004) Neuronal circuits of the neocortex. Ann Rev Neurosci 27:419–451PubMedCrossRefGoogle Scholar
  11. Foeller E, Vater N, Kössl M (2001) Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2:279–296PubMedGoogle Scholar
  12. Heil P (2004) First-spike latency of auditory neurons revisited. Curr Opin Neurobiol 14:461–467PubMedCrossRefGoogle Scholar
  13. Horton JC, Adams DL (2005) The cortical column: a structure without a function. Philos Trans R Soc B 360:837–862CrossRefGoogle Scholar
  14. Huang CL, Winer JA (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J Comp Neurol 427:302–331PubMedCrossRefGoogle Scholar
  15. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol (Lond) 160:106–154Google Scholar
  16. Kaur S, Rose HJ, Lazar R, Liang K, Metherate R (2005) Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro. Neuroscience 134:1033–1045PubMedCrossRefGoogle Scholar
  17. Kelly JP, Wong D (1981) Laminar connections of the cat’s auditory cortex. Brain Res 212:1–15PubMedCrossRefGoogle Scholar
  18. Kimura A, Donishi T, Sakoda T, Hazama M, Tamai Y (2003) Auditory thalamic nuclei projections to the temporal cortex in the rat. Neuroscience 117:1003–1016PubMedCrossRefGoogle Scholar
  19. Kurt S, Crook JM, Ohl FW, Scheich H, Schulze H (2006) Differential effects of iontophoretic in vivo application of the GABAA-antagonists bicuculline and gabazine in sensory cortex. Hear Res 212:224–235PubMedCrossRefGoogle Scholar
  20. Linden JF, Schreiner CE (2003) Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb Cortex 13:83–89PubMedCrossRefGoogle Scholar
  21. Lomber SG, Payne BR (2000) Translaminar differentiation of visually guided behaviours revealed by restricted cerebral cooling deactivation. Cereb Cortex 10:1066–1077PubMedCrossRefGoogle Scholar
  22. Martinez LM, Wang Q, Reid RC, Pillai C, Alonso J-M, Sommer FT, Hirsch JA (2005) Receptive field structure varies with layer in the primary visual cortex. Nat Neurosci 8:372–379PubMedCrossRefGoogle Scholar
  23. Mendelson JR, Schreiner CE, Sutter ML (1997) Functional topography of cat primary auditory cortex: response latencies. J Comp Physiol A 181:615–633PubMedCrossRefGoogle Scholar
  24. Mitani A, Shimokouchi M (1985) Neuronal connections in the primary auditory cortex: an electrophysiological study in the cat. J Comp Neurol 235:417–429PubMedCrossRefGoogle Scholar
  25. Mitani A, Shimokouchi M, Itoh K, Nomura S, Kudo M, Mizuno N (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J Comp Neurol 235:430–447PubMedCrossRefGoogle Scholar
  26. Morel A, Garraghty PE, Kaas JH (1993) Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J Comp Neurol 335:437–459PubMedCrossRefGoogle Scholar
  27. Oonishi S, Katsuki Y (1965) Functional organization and integrative mechanism on the auditory cortex of the cat. Jpn J Neurophysiol 15:342–365Google Scholar
  28. Phillips DP, Irvine DRF (1981) Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. J Neurophysiol 45:48–58PubMedGoogle Scholar
  29. Redies H, Sieben U, Creutzfeldt OD (1989) Functional subdivisions in the auditory cortex of the guinea pig. J Comp Neurol 282:473–488PubMedCrossRefGoogle Scholar
  30. Schwark HD, Malpeli JG, Weyand TG, Lee C (1986) Cat area 17. II. Response properties of infragranular layer neurons in the absence of supragranular layer activity. J Neurophysiol 56:1074–1087PubMedGoogle Scholar
  31. Shen J-X, Xu Z-M, Yao Y-D (1999) Evidence for columnar organization in the auditory cortex of the mouse. Hear Res 137:174–177PubMedCrossRefGoogle Scholar
  32. Shulz DE, Cohen S, Haidarliu S, Ahissar E (1997) Differential effects of acetylcholine on neuronal activity and interactions in the auditory cortex of the guinea-pig. Eur J Neurosci 9:396–409PubMedCrossRefGoogle Scholar
  33. Smith PH, Populin LC (2001) Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J Comp Neurol 436:508–519PubMedCrossRefGoogle Scholar
  34. South DA, Weinberger NM (1995) A comparison of tone-evoked response properties of “cluster” recordings and their constituent single cells in the auditory cortex. Brain Res 704:275–288PubMedCrossRefGoogle Scholar
  35. Sugimoto S, Sakurada M, Horikawa J, Taniguchi I (1997) The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils. Hear Res 112:175–185PubMedCrossRefGoogle Scholar
  36. Sutter ML, Schreiner CE, McLean M, O’Connor KN, Loftus WC (1999) Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J Neurophysiol 82:2358–2371PubMedGoogle Scholar
  37. Syka J, Šuta D, Popelář J (2005) Responses to species-specific vocalizations in the auditory cortex of awake and anesthetised guinea pigs. Hear Res 206:177–184PubMedCrossRefGoogle Scholar
  38. Tanaka H, Taniguchi I (1991) Responses of medial geniculate neurons to species-specific vocalized sounds in the guinea-pig. Jpn J Physiol 41:817–829PubMedCrossRefGoogle Scholar
  39. Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cortex 13:5–14PubMedCrossRefGoogle Scholar
  40. Wallace MN, Kitzes LM, Jones EG (1991a) Chemoarchitectonic organization of the cat primary auditory cortex. Exp Brain Res 86:518–526PubMedGoogle Scholar
  41. Wallace MN, Kitzes LM, Jones EG (1991b) Intrinsic inter- and intra-laminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp Brain Res 86:527–544PubMedGoogle Scholar
  42. Wallace MN, Rutkowski RG, Palmer AR (2000) Identification and localisation of auditory areas in guinea pig cortex. Exp Brain Res 132:445–456PubMedCrossRefGoogle Scholar
  43. Wallace MN, Rutkowski RG, Palmer AR (2002) Interconnections of auditory areas in the guinea pig neocortex. Exp Brain Res 143:106–119PubMedCrossRefGoogle Scholar
  44. Wallace MN, Shackleton TM, Anderson LA, Palmer AR (2005) Representation of the purr call in the guinea pig primary auditory cortex. Hear Res 204:115–126PubMedCrossRefGoogle Scholar
  45. Winer JA (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: neuroanatomy. Springer, New York, pp 222–409Google Scholar
  46. Wree A, Zilles K, Schleicher A (1981) A quantitative approach to cytoarchitectonics VII. The areal pattern of the cortex of the guinea pig. Anat Embryol 162:81–103PubMedCrossRefGoogle Scholar
  47. Zhang JP, Nakamoto KT, Kitzes LM (2005) Modulation of level response areas and stimulus selectivity of neurons in cat primary auditory cortex. J Neurophysiol 94:2263–2274PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.MRC Institute of Hearing ResearchUniversity ParkNottinghamUK

Personalised recommendations