Skip to main content
SpringerLink
Log in

Single-unit responses in the auditory cortex of monkeys performing a conditional acousticomotor task

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The general goal of the present study was to assess the response properties to tones of single neurons in the auditory cortex (primary auditory area, A1, and middle lateral auditory belt, ML) of two macaque monkeys while performing an acousticomotor discrimination task requiring a controlled level of attention and motivation. For each neuron, an approximation of the frequency receptive field (FRF) was first established. Second, based on the FRF, sets of paired tone frequencies were defined in which two different tone frequencies had to be associated by the monkey, following a trial and error strategy, to a left or a right key-press with the left arm. After acquisition of the association, the two tones of the pair were presented randomly (“instruction stimulus”) and, if the monkey touched the correct key, the stimulus was repeated (“confirmation stimulus”) and a reward was delivered. The majority of units (63%) had a FRF formed by multiple peaks, whereas 25% and 12% of units exhibited a simple U-shaped FRF and a “mosaic” FRF, composed of several separated zones of response, respectively. Five principal response patterns were observed: On, Off, On-Off, Sustained, and Inhibition. In relation to the acousticomotor association task, some auditory cortical neurons (33%) exhibited a different response to the same stimulus when presented, in the same trials, as instruction or as confirmation. It was also observed that the response to the same instruction stimulus could differ when comparing correct trials with erroneous trials (wrong motor response). In conclusion, the response properties of auditory cortical neurons in behaving monkeys are strongly dependent on the physical parameters of sounds (frequency, intensity, etc.) as indicated by FRF characteristics, but a substantial influence of the behavioral context and performance may also play an important role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A, B.
Fig. 2A, B.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

Similar content being viewed by others

References

  • Adriani M, Maeder P, Meuli R et al. (2003) Sound recognition and localisation in man: specialised cortical networks and acute effects of circumscribed lesions. Exp Brain Res

    Google Scholar 

  • Ahissar E, Abeles M, Ahissar M, Haidarliu S, Vaadia E (1998) Hebbian-like functional plasticity in the auditory cortex of the behaving monkey. Neuropharmacology 37:633–655

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Merzenich MM, Irvine DRF, Clarey JC, Nelson JE (1986) Frequency representation in the auditory cortex of the common marmoset (Callithrix jacchus jacchus). J Comp Neurol 252:175–185

    Google Scholar 

  • Bakin JS, Weinberger NM (1990) Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res 536:271–286

    CAS  PubMed  Google Scholar 

  • Benson DA, Hienz RD, Goldstein MH Jr (1981) Single-unit activity in the auditory cortex of monkeys actively localizing sound sources: spatial tuning and behavioral dependency. Brain Res 219:249–267

    CAS  PubMed  Google Scholar 

  • Bieser A (1998) Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys. Exp Brain Res 122:139–148

    Article  CAS  PubMed  Google Scholar 

  • Bieser A, Muller-Preuss P (1996) Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds. Exp Brain Res 108:273–284

    CAS  PubMed  Google Scholar 

  • Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77:923–943

    CAS  PubMed  Google Scholar 

  • Brosch M, Schulz A, Scheich H (1999) Processing of sound sequences in macaque auditory cortex: response enhancement. J. Neurophysiol 82:1542–1559

    CAS  PubMed  Google Scholar 

  • Brugge JF, Merzenich MM (1973) Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol 36:1138–1159

    CAS  PubMed  Google Scholar 

  • Calford MB, Webster WR, Semple MM (1983) Measurement of frequency selectivity of single neurons in the central auditory pathway. Hear Res 11:395–401

    CAS  PubMed  Google Scholar 

  • Cheung SW, Bedenbaugh PH, Nagarajan SS, Schreiner CE (2001a) Functional organization of squirrel monkey primary auditory cortex: responses to pure tone. J Neurophysiol 85:1732–1749

    CAS  PubMed  Google Scholar 

  • Cheung SW, Nagarajan SS, Bedenbaugh PH et al. (2001b) Auditory cortical neuron response differences under isoflurane versus pentobarbital anesthesia. Hear Res 156:115–127

    CAS  PubMed  Google Scholar 

  • Diamond DM, Weinberger NM (1989) Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. Behav Neurosci 103:471–494

    CAS  PubMed  Google Scholar 

  • Edeline J-M, Weinberger NM (1993) Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav Neurosci 107:82–103

    CAS  PubMed  Google Scholar 

  • Edeline J-M, Pham P, Weinberger NM (1993) Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav Neurosci 107:539–551

    CAS  PubMed  Google Scholar 

  • Fishman YI, Reser DH, Arezzo JC, Steinschneider M (2000) Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness. J Acoust Soc Am 108:235–246

    CAS  PubMed  Google Scholar 

  • Funkenstein HH, Winter P (1973) Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys. Exp Brain Res 18:464–488

    CAS  PubMed  Google Scholar 

  • Gaese BH, Ostwald J (2001) Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. J Neurophysiol 86:1062–1066

    CAS  PubMed  Google Scholar 

  • Glass I, Wollberg Z (1979) Lability in the responses of cells in the auditory cortex of squirrel monkeys to species-specific vocalizations. Exp Brain Res 34:489–498

    CAS  PubMed  Google Scholar 

  • Hackett TA, Stepniewska I, Kaas JH (1998) Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 394:475–495

    Article  CAS  PubMed  Google Scholar 

  • Hackett TA, Preuss TM, Kaas JH (2001) Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol 441:197–222

    Google Scholar 

  • Hikosaka K, Watanabe M (2000) Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cereb Cortex 10:263–271

    CAS  PubMed  Google Scholar 

  • Hocherman S, Itzhaki A, Gilat E (1981) The response of single units in the auditory cortex of rhesus monkeys to predicted and to unpredicted sound stimuli. Brain Res 230:65–86

    CAS  PubMed  Google Scholar 

  • Imig TS, Ruggero MA, Kitzes LM, Javel E, Brugge JF (1977) Organization of auditory cortex in the owl monkey. J Comp Neurol 171:111–128

    CAS  PubMed  Google Scholar 

  • Kaas JH, Hackett TA (1999) “What” and “where” processing in the auditory cortex. Nat Neurosci 2:1045–1047

    CAS  PubMed  Google Scholar 

  • Kermadi I, Liu Y, Tempini A, Calciati E, Rouiller EM (1998) Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens Mot Res 15:287–308

    CAS  PubMed  Google Scholar 

  • Kiang NYS (1965) Stimulus coding in the auditory nerve and cochlear nucleus. Acta Otolaryngol 59:186–200

    Google Scholar 

  • Kiang NYS, Pfeiffer RR, Warr WB, Backus ASN (1965) Stimulus coding in the cochlear nucleus. Ann Otol Rhinol Laryngol 74:463–485

    CAS  PubMed  Google Scholar 

  • Kisley MA, Gerstein GL (1999) Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex. J Neurosci 19:10451–10460

    CAS  PubMed  Google Scholar 

  • Kisley MA, Gerstein GL (2001) Daily variation and appetitive conditioning-induced plasticity of auditory cortex receptive fields. Eur J Neurosci 13:1993–2003

    Article  CAS  PubMed  Google Scholar 

  • Kosaki H, Hashikawa T, He J, Jones EG (1997) Tonotopic organization of auditory cortical field delineated by parvalbumin immunoreactivity in macaque monkeys. J Comp Neurol 386:304–316

    Article  CAS  PubMed  Google Scholar 

  • Liang L, Lu T, Wang X (2002) Neural representation of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. J Neurophysiol 87:2237–2261

    PubMed  Google Scholar 

  • Luethke LE, Krubitzer LA, Kaas JH (1989) Connections of primary auditory cortex in the new world monkey (Saguinus). J Comp Neurol 285:487–513

    Google Scholar 

  • Maeder P, Meuli R, Adriani M et al. (2001) Distinct pathways involved in sound recognition and localization: a human fMRI study. Neuroimage 14:802–816

    CAS  PubMed  Google Scholar 

  • Manley JA, Muller-Preuss P (1978) Response variability of auditory cortex cells in the squirrel monkey to constant acoustic stimuli. Exp Brain Res 32:171–180

    CAS  PubMed  Google Scholar 

  • Merzenich MM, Brugge JF (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res 50:275–296

    CAS  PubMed  Google Scholar 

  • Merzenich MM, Knight PL, Roth GL (1975) Representation of the cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231–249

    CAS  PubMed  Google Scholar 

  • Miller JM, Sutton D, Pfingst B et al. (1972) Single-cell activity in the auditory cortex of rhesus monkeys: behavioral dependency. Science 177:449–451

    CAS  PubMed  Google Scholar 

  • Morel A, Kaas JH (1992) Subdivisions and connections of auditory cortex in owl monkeys. J Comp Neurol 318:27–63

    Google Scholar 

  • Morel A, Garraghty PE, Kaas JH (1993) Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. J Comp Neurol 335:437–459

    CAS  PubMed  Google Scholar 

  • Nagarajan SS, Cheung SW, Bedenbaugh P et al. (2002) Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. J Neurophysiol 87:1723–1737

    PubMed  Google Scholar 

  • Ohl FW, Scheich H (1997) Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil. J Comp Physiol [A] 181:685–696

    Google Scholar 

  • Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Academic, London, pp 1–165

  • Pelleg-Toiba R, Wollberg Z (1989) Tuning properties of auditory cortex cells in the awake squirrel monkey. Exp Brain Res 74:353–364

    CAS  PubMed  Google Scholar 

  • Pelleg-Toiba R, Wollberg Z (1991) Discrimination of communication calls in the squirrel monkey: “call detectors” or “cell ensembles”? J Basic Clin Physiol Pharmacol 2:257–272

    CAS  PubMed  Google Scholar 

  • Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp Brain Res 1:220–235

    CAS  PubMed  Google Scholar 

  • Pfeiffer RR, Kiang NYS (1965) Spike discharge pattern of spontaneous and continuously stimulated activity in the cochlear nucleus of anaesthetized cats. Biophys J 5:301–316

    Google Scholar 

  • Pfingst BE, O’Connor TA (1980) A vertical stereotaxic approach to auditory cortex in the unanesthetized monkey. J Neurosci Methods 2:33–45

    Article  CAS  PubMed  Google Scholar 

  • Pfingst BE, O’Connor TA (1981) Characteristics of neurons in auditory cortex of monkeys performing a simple auditory task. J Neurophysiol 45:16–34

    CAS  PubMed  Google Scholar 

  • Pfingst BE, O’Connor TA, Miller JM (1977) Response plasticity of neurons in auditory cortex of the rhesus monkey. Exp Brain Res 29:393–404

    CAS  PubMed  Google Scholar 

  • Rauschecker JP (1998a) Cortical processing of complex sounds. Curr Opin Neurobiol 8:516–521

    CAS  PubMed  Google Scholar 

  • Rauschecker JP (1998b) Parallel processing in the auditory cortex of primates. Audio Neurootol 3:86–103

    Article  CAS  Google Scholar 

  • Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of “what” and “where” in the auditory cortex. Proc Natl Acad Sci USA 97(22):11800–11806

    Article  CAS  PubMed  Google Scholar 

  • Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268:111–114

    CAS  PubMed  Google Scholar 

  • Rauschecker JP, Tian B, Pons T, Mishkin M (1997) Serial and parallel processing in rhesus monkey auditory cortex. J Comp Neurol 382:89–103

    CAS  PubMed  Google Scholar 

  • Reale RA, Imig TJ (1980) Tonotopic organization in auditory cortex of the cat. J Comp Neurol 192:265–291

    CAS  PubMed  Google Scholar 

  • Recanzone GH (2000a) Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys. Hear Res 150:104–118

    Article  CAS  PubMed  Google Scholar 

  • Recanzone GH (2000b) Spatial processing in the auditory cortex of the macaque monkey. PNAS 97:11829–11835

    Article  CAS  PubMed  Google Scholar 

  • Recanzone GH, Schreiner CE, Sutter ML, Beitel RE, Merzenich MM (1999) Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey. J Comp Neurol 415:460–481

    Article  CAS  PubMed  Google Scholar 

  • Recanzone GH, Guard DC, Phan ML (2000a) Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. J Neurophysiol 83:2315–2331

    CAS  PubMed  Google Scholar 

  • Recanzone GH, Guard DC, Phan ML, Su T-I K (2000b) Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. J Neurophysiol 83:2723–2739

    CAS  PubMed  Google Scholar 

  • Rhode WS, Kettner RE (1987) Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. J Neurophysiol 57:414–442

    Google Scholar 

  • Romanski LM, Bates JF, Goldman-Rakic PS (1999a) Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403:141–157

    Article  CAS  PubMed  Google Scholar 

  • Romanski LM, Tian B, Fritz J et al. (1999b) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2:1131–1136

    CAS  PubMed  Google Scholar 

  • Ryan A, Miller J (1977) Effects of behavioral performance on single-unit firing patterns in inferior colliculus of the rhesus monkey. J Neurophysiol 40:943–956

    CAS  PubMed  Google Scholar 

  • Ryan A, Miller J (1978) Single-unit responses in the inferior colliculus of the awake and performing rhesus monkey. Exp Brain Res 32:389–407

    Google Scholar 

  • Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10:272–283

    Article  CAS  PubMed  Google Scholar 

  • Schwarz DWF, Tomlinson RWW (1990) Spectral response patterns of auditory cortex neurons to harmonic complex tones in alert monkey (Macaca mulatta). J Neurophysiol 64:282–298

    CAS  PubMed  Google Scholar 

  • Shima K, Tanji J (1998) Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282:1335–1338

    Article  CAS  PubMed  Google Scholar 

  • Sutter ML (2000) Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. J Neurophysiol 84:1012–1025

    CAS  PubMed  Google Scholar 

  • Tian B, Reser D, Durham A, Kustov A, Rauschecker JP (2001) Functional specialization in rhesus monkey auditory cortex. Science 292:290–293

    Google Scholar 

  • Vaadia E, Gottlieb Y, Abeles M (1982) Single-unit activity related to sensorimotor association in auditory cortex of a monkey. J Neurophysiol 48:1210–1213

    Google Scholar 

  • Wang X, Kadia SC (2001) Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. J Neurophysiol 86:2616–2620

    CAS  PubMed  Google Scholar 

  • Wang X, Merzenich MM, Beitel R, Schreiner CE (1995) Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74:2685–2706

    CAS  PubMed  Google Scholar 

  • Wannier T, Liu J, Morel A, Jouffrais C, Rouiller EM (2002) Neuronal activity in primate striatum and pallidum related to bimanual motor actions. Neuroreport 13:143–147

    PubMed  Google Scholar 

  • Weinberger NM, Javid R, Lepan B (1993) Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc Natl Acad Sci USA 90:2394–2398

    CAS  PubMed  Google Scholar 

  • Werner-Reiss U, Kelly AK, Trause AS, Underhill AM, Groh JM (2003) Eye position affects activity in primary auditory cortex of primates. Curr Biol 13:554–562

    Article  CAS  PubMed  Google Scholar 

  • Young ED, Robert J-M, Shofner WP (1988) Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60:1–29

    CAS  PubMed  Google Scholar 

  • Zurita P, Villa AEP, Ribaupierre Y de, Ribaupierre F de, Rouiller EM (1994) Changes of single unit activity in the cat’s auditory thalamus and cortex associated to different anesthetic conditions. Neurosci Res 19:303–316

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank V. Moret, F. Tinguely, and C. Roulin for histology; A. Gaillard, B. Aebischer, and E. Regli for designing and building the mechanics and electronics of home-made equipment as well as maintenance; J. Corpataux and B. Morandi for taking care of the animals in the animal room; L. Monney for informatics. The work was supported financially by the Swiss National Science Foundation (grant 31-61857.00) and the National Center for Competence in Research (NCCR, Neural Plasticity and Repair). We thank Dr. Hoogewoud and Mr. Devaud (Cantonal Hospital of Fribourg) for the collection of CT scan data.

Author information

Author notes

  1. Christophe Jouffrais

    Present address: Centre de Recherche Cerveau et Cognition, CNRS-UPS UMR 5549, Université Paul Sabatier, 133 route de Narbonne, 31062, Toulouse Cedex, France

Authors and Affiliations

  1. Division of Physiology and Program in Neurosciences, Department of Medicine, Faculty of Sciences, University of Fribourg, Chemin du Musée 5, 1700, Fribourg, Switzerland

    Caroline Durif, Christophe Jouffrais & Eric M. Rouiller

Authors
  1. Caroline Durif
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christophe Jouffrais
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eric M. Rouiller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric M. Rouiller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Durif, C., Jouffrais, C. & Rouiller, E.M. Single-unit responses in the auditory cortex of monkeys performing a conditional acousticomotor task. Exp Brain Res 153, 614–627 (2003). https://doi.org/10.1007/s00221-003-1613-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1613-3

Keywords

Search

Navigation