PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of procbThe Royal Society PublishingProceedings BAboutBrowse by SubjectAlertsFree Trial
 
Proc Biol Sci. 1998 April 22; 265(1397): 649–657.
PMCID: PMC1689028

Experience-dependent modulation of tonotopic neural responses in human auditory cortex.

Abstract

Experience-dependent plasticity of receptive fields in the auditory cortex has been demonstrated by electrophysiological experiments in animals. In the present study we used PET neuroimaging to measure regional brain activity in volunteer human subjects during discriminatory classical conditioning of high (8000 Hz) or low (200 Hz) frequency tones by an aversive 100 dB white noise burst. Conditioning-related, frequency-specific modulation of tonotopic neural responses in the auditory cortex was observed. The modulated regions of the auditory cortex positively covaried with activity in the amygdala, basal forebrain and orbitofrontal cortex, and showed context-specific functional interactions with the medial geniculate nucleus. These results accord with animal single-unit data and support neurobiological models of auditory conditioning and value-dependent neural selection.

Full Text

The Full Text of this article is available as a PDF (278K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ashe JH, McKenna TM, Weinberger NM. Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency-specific effects of anticholinesterases provide evidence for a modulatory action of endogenous ACh. Synapse. 1989;4(1):44–54. [PubMed]
  • Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science. 1995 Aug 25;269(5227):1115–1118. [PubMed]
  • Bigl V, Woolf NJ, Butcher LL. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull. 1982 Jun;8(6):727–749. [PubMed]
  • Campeau S, Davis M. Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci. 1995 Mar;15(3 Pt 2):2301–2311. [PubMed]
  • Edeline JM, Weinberger NM. Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. Behav Neurosci. 1991 Oct;105(5):618–639. [PubMed]
  • Edeline JM, Weinberger NM. 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. 1992 Feb;106(1):81–105. [PubMed]
  • Edeline JM, Weinberger NM. Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav Neurosci. 1993 Feb;107(1):82–103. [PubMed]
  • Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. Increased cortical representation of the fingers of the left hand in string players. Science. 1995 Oct 13;270(5234):305–307. [PubMed]
  • Fox K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci. 1992 May;12(5):1826–1838. [PubMed]
  • Friston KJ, Tononi G, Reeke GN, Jr, Sporns O, Edelman GM. Value-dependent selection in the brain: simulation in a synthetic neural model. Neuroscience. 1994 Mar;59(2):229–243. [PubMed]
  • Hars B, Maho C, Edeline JM, Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience. 1993 Sep;56(1):61–74. [PubMed]
  • Hubel DH, Wiesel TN. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. 1970 Feb;206(2):419–436. [PubMed]
  • Jones B, Mishkin M. Limbic lesions and the problem of stimulus--reinforcement associations. Exp Neurol. 1972 Aug;36(2):362–377. [PubMed]
  • Jones EG, Powell TP. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain. 1970;93(4):793–820. [PubMed]
  • Krettek JE, Price JL. A direct input from the amygdala to the thalamus and the cerebral cortex. Brain Res. 1974 Feb 15;67(1):169–174. [PubMed]
  • Krettek JE, Price JL. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol. 1977 Jan 15;171(2):157–191. [PubMed]
  • LaBar KS, LeDoux JE, Spencer DD, Phelps EA. Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci. 1995 Oct;15(10):6846–6855. [PubMed]
  • LeDoux JE, Sakaguchi A, Reis DJ. Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci. 1984 Mar;4(3):683–698. [PubMed]
  • LeDoux JE, Ruggiero DA, Reis DJ. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol. 1985 Dec 8;242(2):182–213. [PubMed]
  • LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci. 1988 Jul;8(7):2517–2529. [PubMed]
  • McIntosh AR, Gonzalez-Lima F. Functional network interactions between parallel auditory pathways during Pavlovian conditioned inhibition. Brain Res. 1995 Jun 19;683(2):228–241. [PubMed]
  • McKenna TM, Ashe JH, Weinberger NM. Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency-specific effects of muscarinic agonists. Synapse. 1989;4(1):30–43. [PubMed]
  • Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience. 1983 Jan;8(1):33–55. [PubMed]
  • Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol. 1984 Apr 20;224(4):591–605. [PubMed]
  • Mesulam MM, Mufson EJ, Levey AI, Wainer BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol. 1983 Feb 20;214(2):170–197. [PubMed]
  • Metherate R, Ashe JH. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 1991 Sep 13;559(1):163–167. [PubMed]
  • Metherate R, Weinberger NM. Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse. 1990;6(2):133–145. [PubMed]
  • Morel A, Garraghty PE, Kaas JH. Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J Comp Neurol. 1993 Sep 15;335(3):437–459. [PubMed]
  • Morris JS, Friston KJ, Dolan RJ. Neural responses to salient visual stimuli. Proc Biol Sci. 1997 May 22;264(1382):769–775. [PMC free article] [PubMed]
  • Pantev C, Roberts LE, Elbert T, Ross B, Wienbruch C. Tonotopic organization of the sources of human auditory steady-state responses. Hear Res. 1996 Nov 1;101(1-2):62–74. [PubMed]
  • Penhune VB, Zatorre RJ, MacDonald JD, Evans AC. Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex. 1996 Sep-Oct;6(5):661–672. [PubMed]
  • Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. Massive cortical reorganization after sensory deafferentation in adult macaques. Science. 1991 Jun 28;252(5014):1857–1860. [PubMed]
  • Recanzone GH, Schreiner CE, Merzenich MM. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci. 1993 Jan;13(1):87–103. [PubMed]
  • Roberts AC, Robbins TW, Everitt BJ, Muir JL. A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets. Neuroscience. 1992;47(2):251–264. [PubMed]
  • Russchen FT, Bakst I, Amaral DG, Price JL. The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res. 1985 Mar 11;329(1-2):241–257. [PubMed]
  • Scheich H, Simonis C, Ohl F, Tillein J, Thomas H. Functional organization and learning-related plasticity in auditory cortex of the Mongolian gerbil. Prog Brain Res. 1993;97:135–143. [PubMed]
  • Schreurs BG, McIntosh AR, Bahro M, Herscovitch P, Sunderland T, Molchan SE. Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J Neurophysiol. 1997 Apr;77(4):2153–2163. [PubMed]
  • Seltzer B, Pandya DN. Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. J Comp Neurol. 1989 Mar 1;281(1):97–113. [PubMed]
  • Thorpe SJ, Rolls ET, Maddison S. The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res. 1983;49(1):93–115. [PubMed]
  • Weinberger NM, Diamond DM. Physiological plasticity in auditory cortex: rapid induction by learning. Prog Neurobiol. 1987;29(1):1–55. [PubMed]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society