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Neural connectivity only accounts for a small part of neural correlation in auditory cortex

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Abstract

In order to allow the relation of functional connectivity patterns (inferred from cross-correlograms) to structural connectivity (the anatomical substrate), we analyzed cross-correlogram peaks for spontaneous and stimulated activity in the auditory cortex. It was assumed that the broad correlograms, usually encountered, represent neural connectivity as well as secondary effects such as intrinsic firing patterns, global synchrony related to the ongoing electroencephalographic activity, and stimulus-related effects. Data were collected from 604 neuron pairs recorded under spontaneous conditions in primary auditory cortex of seven juvenile (30–70 days) and nine adult cats. Three hundred and six pairs (51%) had a peak cross-correlation coefficient significantly different from zero. For 113 neuron pairs out of this subgroup, correlations were calculated also for spike trains recorded during click stimulation. After a combined burst-correction and deconvolution procedure was carried out, the correlation peak strengths were not significantly changed for spontaneous activity, but peak width was narrower for single-electrode pairs than for dual-electrode pairs, suggesting a better synchronization for neighboring neurons. Under click stimulation conditions, overall peak synchronization strength was independent of interelectrode distance, whereas, after correction for secondary and stimulus effects, peak synchronization was significantly lower for dual-electrode pairs. However, the primary peak width for single-electrode pairs under stimulus conditions was no longer different from that of dual-electrode pairs. This implies that both under spontaneous and stimulus conditions secondary effects largely obscure any underlying correlation produced by anatomical connectivity. The secondary effects may be the result of intrinsic as well as network properties in auditory cortex and may functionally be more important than the weak primary effects resulting from anatomical connections. Cross-interval analysis suggests that the correlations in auditory cortex are dynamic and may show random switching between states of stronger and weaker synchronization.

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References

  • Abeles M (1982) Local cortical circuits. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Aertsen A, Arndt M (1993) Response synchronization in the visual cortex. Curr Opin Neurobiol 3: 586–594

    Google Scholar 

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

    Google Scholar 

  • Bendat JS, Piersol AG (1971) Random data: analysis and measurement procedures. Wiley, New York

    Google Scholar 

  • Bowman DM, Eggermont JJ, Smith GM (1995) The effect of stimulation on burst firing in cat primary auditory cortex. J Neurophysiol 74: 1841–1855

    Google Scholar 

  • Brillinger DR, Bryant HL, Segundo JP (1976) Identification of synaptic interactions. Biol Cybern 22: 213–228

    Google Scholar 

  • Brosch M, Schreiner CE (1995) Correlated neural activity in the iso-frequency domain of cat primary auditory cortex (abstract). Association for Research in Otolaryngology, ARO 525: 132

    Google Scholar 

  • Dickson JW, Gerstein GL (1974) Interaction between neurons in auditory cortex of the cat. J Neurophysiol 37: 1239–1261

    Google Scholar 

  • Eckhorn R, Obermueller A (1993) Single neurons are differently involved in stimulus-specific oscillations in cat visual cortex. Exp Brain Res 95: 177–182

    Google Scholar 

  • Eggermont JJ (1988) On the interpretation of neural interaction in the auditory nervous system. In: Duifhuis H, Horst JW, Wit HP (eds) Basic issues in hearing. Academic, London, pp 270–278

    Google Scholar 

  • Eggermont JJ (1991) Rate and synchronization measures of periodicity coding in cat primary auditory cortex. Hearing Res 56: 153–167

    Google Scholar 

  • Eggermont JJ (1992) Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation and age. J Neurophysiol 68: 1216–1228

    Google Scholar 

  • Eggermont JJ (1994) Neural interaction in cat primary auditory cortex. II. Effects of sound stimulation. J Neurophysiol 71: 246–270

    Google Scholar 

  • Eggermont JJ, Smith GM (1995a) Separating local from global effects in neural pair correlograms. Neuroreport 6: 2121–2124

    Google Scholar 

  • Eggermont JJ, Smith GM (1995b) Rate covariance dominates spontaneous cortical unit-pair correlograms. Neuroreport 6: 2125–2128

    Google Scholar 

  • Eggermont JJ, Smith GM, Bowman D (1993) Spontaneous burst firing in cat primary auditory cortex. Age and depth dependence and its effect on neural interaction measures. J Neurophysiol 69: 1292–1313

    Google Scholar 

  • Erb M, Aertsen A, Palm G (1990) Functional connectivity in neuronal systems: context-dependence of effective network organization does not require synaptic plasticity. In: Elsner N, Roth G (eds) Brain perception cognition. Thieme, Stuttgart, pp 527

    Google Scholar 

  • Fetz E, Shupe LE (1994) Measuring synaptic interactions. Science 263: 1295–1296

    Google Scholar 

  • Fetz E, Toyama K, Smith W (1991) Synaptic interactions between cortical neurons. In: Peters A, Jones EG (eds) Normal and altered states of function. (Cerebral cortex, vol 9) Plenum, New York, pp 1–47

    Google Scholar 

  • Gerstein GL (1970) Functional associations of neurons: detection and interpretation. In: Schmitt FO (ed) The neurosciences: second study program. Rockefeller University Press, New York, pp 648–661

    Google Scholar 

  • Gochin PM, Miller EK, Gross CG, Gerstein GL (1991) Functional interactions among neurons in inferior temporal cortex of the awake macaque. Exp Brain Res 84: 505–516

    Google Scholar 

  • Heierli P, Ribaupierre F de, Ribaupierre Y de (1987) Functional properties and interactions of neuron pairs simultaneously recorded in the medial geniculate body of the cat. Hearing Res 25: 209–225

    Google Scholar 

  • Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376: 33–36

    Google Scholar 

  • Johnson DH, Kiang NY-S (1976) Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys J 16: 719–734

    Google Scholar 

  • Krüger J (1991) Spike train correlation on slow time scales in monkey visual cortex. In: Krüger J (ed) Neuronal cooperativity. Springer, Berlin Heidelberg New York, pp 105–132

    Google Scholar 

  • Krüger J, Aiple F (1988) (1988) Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. J Neurophysiol 60: 798–828

    Google Scholar 

  • Krüger J, Mayer M (1990) Two types of neuronal synchrony in monkey striate cortex. Biol Cybern 64: 135–140

    Google Scholar 

  • Legéndy 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 

  • Malsburg C von der (1981) The correlation theory of brain function. Internal Report 81-2, Department of Neurobiology, MaxPlanck-Institute for Biophysical Chemistry, pp 1–38

  • 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 

  • McCormick DA, Feeser HR (1990) Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39: 103–113

    Google Scholar 

  • Melssen WJ, Epping WJM (1987) Detection and estimation of neural connectivity based on crosscorrelation analysis. Biol Cybern 57: 403–414

    Google Scholar 

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

    Google Scholar 

  • Nelson JI, Salin PA, Munk MH-J, Arzi M, Bullier J (1992) Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17 and 18 in the cat. Vis Neurosci 9: 21–37

    Google Scholar 

  • Perkel DH (1970) Spike trains as carriers of information. In: Schmitt FO (ed) The neurosciences: second study program. Rockefeller University Press, New York, pp 587–596

    Google Scholar 

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

    Google Scholar 

  • Recanzone GH, Merzenich MM, Dinse HR (1992) Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. Cereb Cortex 2: 181–196

    Google Scholar 

  • Rotter S, Aertsen A, Vaadia E (1993) Neuronal interaction in the cortex quantitative characterization by cross-interval statistics. In: Aertsen A (ed) Brain theory. Elsevier Science, Amsterdam, pp 231–239

    Google Scholar 

  • Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55: 349–374

    Article  CAS  PubMed  Google Scholar 

  • Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17: 119–130

    Google Scholar 

  • Toyama K, Tanaka K (1984) Visual cortical function studied by cross correlation analysis. In: Edelman GM, Gall WE, Cowan WE (eds) Dynamic aspects of neocortical function. Wiley New York, pp 67–86

    Google Scholar 

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

    Google Scholar 

  • Toyama K, Kimura M, Tanaka K (1981b) Organization of cat visual cortex as investigated by cross-correlation technique. J Neurophysiol 46: 202–214

    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 

  • Vaadia E, Bergman H, Abeles M (1989) Neuronal activities related to higher brain functions theoretical and experimental implications. IEEE Trans Biomed Eng 36: 25–35

    Google Scholar 

  • Vaadia E, Ahissar E, Bergman H, Lavner Y (1991) Correlated activity of neurons: a neural code for higher brain functions. In: Krüger J (ed) Neuronal cooperativity. Springer, Berlin Heidelberg New York, pp 249–279

    Google Scholar 

  • Wallace MN, Kitzes LM, Jones EG (1991) Intrinsic interand intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp Brain Res 86: 527–544

    Google Scholar 

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Eggermont, J.J., Smith, G.M. Neural connectivity only accounts for a small part of neural correlation in auditory cortex. Exp Brain Res 110, 379–391 (1996). https://doi.org/10.1007/BF00229138

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