Skip to main content
Log in

Functional interactions among neurons in inferior temporal cortex of the awake macaque

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Functional interactions among inferior temporal cortex (IT) neurons were studied in the awake, fixating macaque monkey during the presentation of visual stimuli. Extracellular recordings were obtained simultaneously from several microelectrodes, and in many cases, spike trains from more than one neuron were extracted from each electrode by the use of spike shape sorting technology. Functional interactions between pairs of neurons were measured using cross-correlation. Discharge patterns of single neurons were evaluated using auto-correlation and PST histograms. Neurons recorded on the same electrode (within about 100 μn) had more similar stimulus selectivity and were more likely to show functional interactions than those recorded on different electrodes spaced about 250 to 500 microns apart. Most neurons tended to fire in bursts tens to hundreds of milliseconds in duration, and asynchronously from the stimulus induced rate changes. Correlated neuronal firing indicative of shared inputs and direct interactions was observed. Occurrence of shared input was significantly lower for neuron pairs recorded on different electrodes than for neurons recorded on the same electrode. Direct connections occurred about as often for neurons on different electrodes as for neurons on the same electrode. These results suggest that input projections are usually restricted to less than 500 μm patches and are then distributed over greater distances by intrinsic connections. Measurements of synaptic contribution suggest that typically more than 5 near-simultaneous inputs are required to cause an IT neuron to discharge.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abeles M (1982a) Quantification, smoothing, and confidence limits for single-units' histograms. J Neurosci Meth 5:317–325

    Google Scholar 

  • Abeles M (1982b) Local cortical circuits: an electrophysiological study. Studies of brain function, Vol 6. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Abeles M, Goldstein M (1977) Multispike train analysis. Proc IEEE 65:762–773

    Google Scholar 

  • Aertsen A, Gerstein GL (1985) Evaluation of neuronal connectivity: sensitivity of crosscorrelation. Brain Res 340:341–354

    Google Scholar 

  • Aertsen AMHJ, Gerstein GL, Habib MK, Palm G, Gochin P, Kruger J (1989) Dynamics of neuronal firing correlation: modulation of “effective connectivity”. J Neurophysiol 61:900–917

    Google Scholar 

  • Baylis GC, Rolls ET, Leonard CM (1978) Functional subdivisions of temporal lobe neocortex. J Neurosci 7:330–342

    Google Scholar 

  • Bedenbaugh PH, Gerstein GL, Boven KH, Aertsen AMHJ (1988) The meaning of stimulus dependent changes in cross correlation between neural spike trains. Neuroscience Abstr 14:651

    Google Scholar 

  • Boven K-H, Aertsen A (1990) Dynamics of activity in neuronal networks give rise to fast modulations of functional connectivity. In: Eckmiller R et al (eds) Parallel processing in neuronal systems and computers. Elsevier, Amsterdam, pp 53–56

    Google Scholar 

  • Byrant HL, Marcos AR, Segundo JP (1973) Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. J Neurophysiol 36:205–255

    Google Scholar 

  • Creutzfeldt O, Ito M (1968) Functional synaptic organization of primary visual cortex neurons in the cat. Exp Brain Res 6:324–352

    Google Scholar 

  • Desimone R, Gross CG (1979) Visual areas in the temporal cortex of the macaque. Brain Res 178:363–380

    Google Scholar 

  • Desimone R, Albright TD, Gross CG, Bruce C (1984) Stimulus selective properties of inferior temporal neurons in the macaque. J Neurosci 4:2051–2062

    Google Scholar 

  • Fuster JM, Jervey JP (1982) Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. J Neurosci 2:361–375

    Google Scholar 

  • Gerstein G, Bedenbaugh P, Aertsen A (1989) Neuronal assemblies. IEEE Trans Biomed Eng 36:4–14

    Google Scholar 

  • Gerstein G, Bloom M, Espinosa U, Evanczuk S, Turner M (1983) Design of a laboratory for multi-neuron studies. IEEE Trans Syst Man Cybern 13:668–676

    Google Scholar 

  • Gochin PM (1990) Pattern recognition in primate temporal cortex: but is it ART?. Proc Int Joint Conf Neural Networks 1:177–79

    Google Scholar 

  • Gochin PM, Lubin JM (1990) A hierarchical machine vision system based on a model of the primate visual system. Proc IEEE Int Symp Intelligent Control (in press)

  • Gochin PM, Kaltenbach JA, Gerstein GL (1989) Coordinated activity of neuron pairs in anesthetized rat dorsal cochlear nucleus. Brain Res 497:1–11

    Google Scholar 

  • Gochin PM, Miller EK, Gross CG (1988) Circuit properties of inferior temporal cortex in the macaque. Neuroscience Abstr 14:11

    Google Scholar 

  • Gross CG (1973) Visual functions of inferotemporal cortex. In: Jung R (ed) Handbook of sensory physiology, Vol 7, Part 3B. Springer, Berlin, pp 451–482

    Google Scholar 

  • Gross CG, Bender DB, Gerstein GL (1979) Activity of inferior temporal neurons in behaving monkeys. Neuropsychology 17:215–229

    Google Scholar 

  • Gross CG, Mishkin M (1977) The neural basis of stimulus equivalence across retinal translation. In: Harnad S, Doty R, Jaynes J, Goldstein L, Krauthamer G (eds) Lateralization in the nervous system. Academic Press, New York, pp 109–122

    Google Scholar 

  • Gross CG, Rocha-Miranda CE, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the macaque. J Neurophysiol 35:96–111

    Google Scholar 

  • Grossberg S (1987) Competitive learning: from interactive activation to adaptive resonance. Cognitive Sci 11:23–63

    Google Scholar 

  • Hata Y, Tsumoto T, Sato H, Hagihara K, Tamura H (1988) Inhibition contributes to orientation selectivity in visual cortex of the cat. Nature 335:815–817

    Google Scholar 

  • Komatsu Y, Nakajima S, Toyama K, Fetz E (1988) Introcortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex. Brain Res 442:359–62

    Google Scholar 

  • Kruger J, Aiple F (1988) Multi-microelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. J Neurophysiol 80:798–828

    Google Scholar 

  • Legendy CR, Salcman M (1985) Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53:926–939

    Google Scholar 

  • Levick WR, Cleland BG, Dubin MW (1972) Lateral geniculate neurons of the cat: retinal inputs and physiology. Invest Opthalmol 11:302–311

    Google Scholar 

  • Mastronarde DN (1983) Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J Neurophysiol 49:325–349

    Google Scholar 

  • Michalski A, Gerstein GL, Czarkowska J, Tarnecki R (1983) Interactions between cat striate cortex neurons. Exp Brain Res 51:97–107

    Google Scholar 

  • Miller EK, Gochin PM, Gross CG, Gerstein GL (1989) Attenuation of responses of inferior temporal neurons in awake monkeys by addition of a second stimulus. Neuroscience Abstr 15:163

    Google Scholar 

  • Mishkin M (1982) A memory system in the monkey. Philos Trans R Soc Lond B298:85–95

    Google Scholar 

  • Moran J, Desimone D (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229:782–784

    Google Scholar 

  • Moore GP, Segundo JP, Perkel DH, Levitan H (1970) Statistical signs of synaptic interaction in neurons. Biophys J 10:876–900

    Google Scholar 

  • Mountcastle VB, Davies PW, Berman AL (1957) Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli. J Neurophysiol 20:374–407

    Google Scholar 

  • Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419–440

    Google Scholar 

  • Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145

    CAS  PubMed  Google Scholar 

  • Sarna MF, Gochin PM, Kaltenbach J, Salganicoff, Gerstein GL (1988) Unsupervised waveform classification for multi-neuron recordings: a real-time, software based system. II. Performance comparison to other sorters. J Neurosci Meth 25:189–196

    Google Scholar 

  • Schwartz EL, Desimone R, Albright TD, Gross CG (1983) Shape recognition and inferior temporal neurons. Proc Nat Acad Sci 80:5776–5778

    Google Scholar 

  • Spitzer H, Desimone R, Moran J (1988) Increased attention enhances both behavioral and neuronal performance. Science 240:338–340

    Google Scholar 

  • Toyama K, Kimura M, Tanaka K (1981) Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J Neurophysiol 46:191–201

    Google Scholar 

  • Ts'o DY, Gilbert CD, Wiesel TN (1986) Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6:1160–1170

    Google Scholar 

  • Ts'o DY, Gilbert CD (1988) The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci 8:1712–1727

    Google Scholar 

  • Tsumoto T, Creutzfeldt OD, Legendy CR (1978) Functional organization of the corticofugal system from the visual cortex to the lateral geniculate nucleus in the cat. Exp Brain Res 32:345–364

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gochin, P.M., Miller, E.K., Gross, C.G. et al. Functional interactions among neurons in inferior temporal cortex of the awake macaque. Exp Brain Res 84, 505–516 (1991). https://doi.org/10.1007/BF00230962

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00230962

Key words

Navigation