Abstract
The auditory system consists of the ascending and descending (corticofugal) systems. The corticofugal system forms multiple feedback loops. Repetitive acoustic or auditory cortical electric stimulation activates the cortical neural net and the corticofugal system and evokes cortical plastic changes as well as subcortical plastic changes. These changes are short-term and are specific to the properties of the acoustic stimulus or electrically stimulated cortical neurons. These plastic changes are modulated by the neuromodulatory system. When the acoustic stimulus becomes behaviorally relevant to the animal through auditory fear conditioning or when the cortical electric stimulation is paired with an electric stimulation of the cholinergic basal forebrain, the cortical plastic changes become larger and long-term, whereas the subcortical changes stay short-term, although they also become larger. Acetylcholine plays an essential role in augmenting the plastic changes and in producing long-term cortical changes. The corticofugal system has multiple functions. One of the most important functions is the improvement and adjustment (reorganization) of subcortical auditory signal processing for cortical signal processing.
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Abbreviations
- AC:
-
Auditory cortex
- ACh:
-
Acetylcholine
- AIp:
-
Posterior division of the primary auditory cortex
- BAZ:
-
Best azimuth
- BDe:
-
Best delay
- BDu:
-
Best duration
- BF:
-
Best frequency
- CM:
-
Cochlear microphonic
- CS:
-
Conditioned stimulus
- DPD:
-
Dorsoposterior division
- DSCF:
-
Doppler-shifted constant frequency
- DSCFd:
-
Dorsal DSCF area
- DSCFv:
-
Ventral DSCF area
- IC:
-
Inferior colliculus
- MGB:
-
Medial geniculate body
- MGBm:
-
Medial division of MGB
- MGBv:
-
Ventral division of MGB
- MT:
-
Minimum threshold
- PIN:
-
Posterior intralaminar nucleus
- US:
-
Unconditioned stimulus
References
Aitkin LM (1973) Medial geniculate body of the cat: responses to tonal stimuli of neurons in medial division. J Neurophysiol 36:275–283
Armony JL, Quirk GJ, LeDoux JE (1998) Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning. J Neurosci 18:2592–2601
Bakin JS, Weinberger NM (1996) Induction of physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci USA 93:11219–11224
Bjordahl TS, Dimyan MA, Weinberger NM (1998) Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behav Neurosci 112:467–479
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 98:261–274
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 98:275–286
Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364
Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847–850
Chowdhury SA, Suga N (2000) Reorganization of the frequency map of the auditory cortex evoked by cortical electrical stimulation in the big brown bat. J Neurophysiol 83:1856–1863
Covey E, Casseday JH (1999) Timing in the auditory system of the bat. Ann Rev Physiol 61:457–476
Cruikshank SJ, Edeline JM, Weinberger NM (1992) Stimulation at a site of auditory–somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. Behav Neurosci 106:471–483
DiCara LV, Braun JJ, Pappas BA (1970) Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. J Comp Physiol Psychol 73:208–216
Edeline JM, Weinberger NM (1991) Subcortical adaptive filtering in the auditory system: associative receptive field plasticity in the dorsal medial geniculate body. Behav Neurosci 105:154–175
Ehrlich D, Casseday JH, Covey E (1997) Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:2360–2372
Galazyuk AV, Feng AS (1997) Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus. J Comp Physiol [A] 180:301–311
Gao E, Suga N (1998) Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci USA 95:12663–12670
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 97:8081–8086
Goldberg RL, Henson OW Jr (1998) Changes in cochlear mechanics during vocalization: evidence for a phasic medial efferent effect. Hear Res 122:71–81
Harrison RV, Ibrahim D, Stanton SG, Mount RJ (1996) Reorganization of frequency maps in chinchilla auditory midbrain after long-term basal cochlear lesions induced at birth. In: Salvi RJ, Hendersen D, Fiorino F, Colletti V (eds) Auditory system plasticity and regeneration, vol 19. Thieme Med. Pub., Inc., New York, pp 238–255
He J (2003) Corticofugal modulation of the auditory thalamus. Exp Brain Res 153:579–590
Heffner HE, Heffner RS (1984) Temporal lobe lesions and perception of species-specific vocalizations by macaques. Science 226:75–76
Huffman RF, Henson OW Jr (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Brain Res Rev 15:295–323
Irvine DRF, Rajan R (1996) Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning. Clin Exp Pharmacol Physiol 23:939–947
Jen PH, Zhou X (2003) Corticofugal modulation of amplitude domain processing in the midbrain of the big brown bat, Eptesicus fuscus. Hear Res 184:91–106
Jen PH, Chen QC, Sun XD (1998) Corticofugal regulation of auditory sensitivity in the bat inferior colliculus. J Comp Physiol [A] 183:683–697
Ji W, Gao E, Suga N (2001) Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J Neurophysiol 86:211–225
Ji W, Suga N (2003) Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. J Neurophysiol 90:1904–1909
Ji W, Suga N (2007a) Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning. J Neurosci 27:4910–4918
Ji W, Suga N (2007b) Cortical tone-specific plasticity elicited by conditioning and cortical non-specific plasticity elicited by pseudoconditioning depend on different neuromodulators and neural circuits. Soc Neurosci Abst
Ji W, Suga N and Gao E (2005) Effects of agonists and antagonists of NMDA and ACh receptors on plasticity of bat auditory system elicited by fear conditioning. J Neurophysiol 94:1199–1211
Kelly JP, Wong D (1981) Laminar connections of the cat’s auditory cortex. Brain Res 212:1–15
Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–1718
Li XF, Stutzmann GE, LeDoux JE (1996) Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. Learn Mem 3:229–242
Liu W, Suga N (1997) Binaural and commissural organization of the primary auditory cortex of the mustached bat. J Comp Physiol [A] 181:599–605
Ma X, Suga N (2001a) Plasticity of bat’s central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. J Neurophysiol 85:1078–1087
Ma X, Suga N (2001b) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc Natl Acad Sci USA 98:14060–14065
Ma X, Suga N (2003) Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J Neurophysiol 89:90–103
Ma X, Suga N (2004) Lateral inhibition for center-surround reorganization of the frequency map of bat auditory cortex. J Neurophysiol 92:3192–3199
Ma X, Suga N (2005) Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci USA 102:9335–9340
Manabe T, Suga N, Ostwald J (1978) Aural representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustache bat. Science 200:339–342
Maren S (2000) Auditory fear conditioning increases CS-elicited spike firing in lateral amygdala neurons even after extensive overtraining. Eur J Neurosci 12:4047–4054
Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844–852
Maren S, Yap SA, Goosens KA (2001) The amygdala is essential for the development of neuronal plasticity in the medial geniculate nucleus during auditory fear conditioning in rats. J Neurosci 21:RC135
Mauk MD, Thompson RF (1987) Retention of classically conditioned eyelid responses following acute decerebration. Brain Res 403:89–95
Mooney DM, Zhang L, Basile C, Senatorov VV, Ngsee J, Omar A, Hu B (2004) Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. Proc Natl Acad Sci USA 101:320–324
Norman RJ, Villablanca JR, Brown KA, Schwafel JA, Buchwald JS (1974) Classical eyeblink conditioning in the bilaterally hemispherectomized cat. Exp Neurol 44:363–380
Ojima H (1994) Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cerebral Cortex 6:646–663
Pinheiro AD, Wu M, Jen PH (1991) Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol [A] 169:69–85
Poremba A, Gabriel M (1997) Medial geniculate lesions block amygdalar and cingulothalamic learning-related neuronal activity. J Neurosci 17:8645–8655
Poremba A, Gabriel M (2001) Amygdalar efferents initiate auditory thalamic discriminative training-induced neuronal activity. J Neurosci 21:270–278
Quirk GJ, Repa C, LeDoux JE (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 15:1029–1039
Quirk GJ, Armony JL, LeDoux JE (1997) Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19:613–624
Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc Natl Acad Sci USA 97:11800–11806
Romanski LM, LeDoux JE (1993) Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cereb Cortex 3:515–532
Saldana E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40
Sakai M, Suga N (2001) Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices. Proc Natl Acad Sci USA 98:3507–3512
Sakai M, Suga N (2002) Centripetal and centrifugal reorganizations of frequency map of the auditory cortex in gerbils. Proc Natl Acad Sci USA 99:7108–7112
Suga N (1973) Feature extraction in the auditory system of bats. In: Moller AR (ed) Basic mechanisms in hearing. Academic, New York, pp 675–742
Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373
Suga N (1994) The processing of auditory information carried by species-specific complex sounds. In: Gazzaniga MS (ed) The cognitive neurosciences. MIT, Cambridge, pp 295–313
Suga N, Jen PH (1976) Disproportionate tonotopic representation for processing CF-FM sonar signals in the mustache bat auditory cortex. Science 194:542–544
Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794
Suga N, Niwa H, Taniguchi I, Margoliash D (1987) The personalized auditory cortex of the mustached bat: adaptation for echolocation. J Neurophysiol 58:643–654
Suga N, Gao E, Zhang Y, Ma X, Olsen JF (2000) The corticofugal system for hearing: recent progress. Proc Natl Acad Sci USA 97:11807–11814
Suga N, Xiao Z, Ma X, Ji W (2002) Plasticity and corticofugal modulation for hearing in adult animals. Neuron 36:9–18
Suga N, Ma X, Gao E, Sakai M, Chowdhury SA (2003) Descending system and plasticity for auditory signal processing: neuroethological data for speech scientists. Speech Commun 41:189–200
Weinberger NM (2004) Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5:279–290
Weinberger NM (1998) Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol Learn Mem 70:226–251
Wenstrup JJ, Ross LS, Pollak GD (1986) Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization. J Neurosci 6:962–973
Wu Y, Yan J (2007) Modulation of the receptive fields of midbrain neurons elicited by thalamic electrical stimulation through corticofugal feedback. J Neurosci (in press)
Xiao Z, Suga N (2002a) Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nat Neurosci 5:57–63
Xiao Z, Suga N (2002b) Reorganization of the cochleotopic map in the bat’s auditory system by inhibition. Proc Natl Acad Sci USA 99:15743–15748
Xiao Z, Suga N (2004) Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat. Proc Natl Acad Sci USA 101:1769–1774
Xiao X, Suga N (2005) Asymmetry in corticofugal modulation of frequency tuning in mustached bat auditory system. Proc Natl Acad Sci USA 102:19162–19167
Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16:1–11
Yan J, Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273:1100–1103
Yan J, Suga N (1999) Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. J Neurophysiol 81:817–24
Yan W, Suga N (1998) Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1:54–58
Yan J, Zhang Y (2005) Sound-guided shaping of the receptive field in the mouse auditory cortex by basal forebrain activation. Eur J Neurosci 21:563–576
Yu YQ, Xiong Y, Chan YS, He J (2004) Corticofugal gating of auditory information in the thalamus: an in vivo intracellular recording study. J Neurosci 24:3060–3069
Zhang Y, Hakes JJ, Bonfield SP, Yan J (2005) Corticofugal feedback for auditory midbrain plasticity elicited by tones and electrical stimulation of basal forebrain in mice. Eur J Neurosci 22:871–879
Zhang Y, Suga N (1997) Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J Neurophysiol 78:3489–3492
Zhang Y, Suga N (2000) Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bat. J Neurophysiol 84:325–333
Zhang Y, Suga N (2005) Corticofugal feedback for collicular plasticity evoked by electric stimulation of the inferior colliculus. J Neurophysiol 94:2676–2682
Zhang Y, Suga N, Yan J (1997) Corticofugal modulation of frequency processing in bat auditory system. Nature 387:900–903
Zhou X, Jen PH (2005) Corticofugal modulation of directional sensitivity in the midbrain of the big brown bat, Eptesicus fuscus. Hear Res 203:201–215
Zook JM, Winer JA, Pollak GD, Bodenhamer RD (1985) Topology of the central nucleus of the mustache bat’s inferior colliculus: correlation of single unit properties and neuronal architecture. J Comp Neurol 231:530–546
Acknowledgments
Our work has been supported by a research grant from the National Institute on Deafness and Other Communication Disorders (DC000175). I thank my present and past collaborators Drs. Syed M. Chowdhury, Enquan Gao, Weiqing Ji, Xiaofeng Ma, Masashi Sakai, Zhongju Xiao, Jun Yan, Wei Yan and Yungfeng Zhang for their excellent research on the function of the corticofugal auditory system and also my laboratory technician, Ms. Sally E. Miller for editing this manuscript.
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Suga, N. Role of corticofugal feedback in hearing. J Comp Physiol A 194, 169–183 (2008). https://doi.org/10.1007/s00359-007-0274-2
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DOI: https://doi.org/10.1007/s00359-007-0274-2