Cortical Representation of Auditory Space: Information-Bearing Features of Spike Patterns

Abstract

Furukawa, Shigeto and John C. Middlebrooks. Cortical representation of auditory space: information-bearing features of spike patterns. J Neurophysiol 87: 1749 -1762, 2002; 10.1152/jn.00491.2001. Previous studies have demonstrated that the spike patterns of cortical neurons vary systematically as a function of sound-source location such that the response of a single neuron can signal the location of a sound source throughout 360°of azimuth. The present study examined specific features of spike patterns that might transmit information related to sound-source location. Analysis was based on responses of well-isolated single units recorded from cortical area A2 in ␣-chloralose-anesthetized cats. Stimuli were 80-ms noise bursts presented from loudspeakers in the horizontal plane; source azimuths ranged through 360°in 20°steps. Spike patterns were averaged across samples of eight trials. A competitive artificial neural network (ANN) identified sound-source locations by recognizing spike patterns; the ANN was trained using the learning vector quantization learning rule. The information about stimulus location that was transmitted by spike patterns was computed from joint stimulus-response probability matrices. Spike patterns were manipulated in various ways to isolate particular features. Full-spike patterns, which contained all spike-count information and spike timing with 100-s precision, transmitted the most stimulus-related information. Transmitted information was sensitive to disruption of spike timing on a scale of more than ϳ4 ms and was reduced by an average of ϳ35% when spike-timing information was obliterated entirely. In a condition in which all but the first spike in each pattern were eliminated, transmitted information decreased by an average of only ϳ11%. In many cases, that condition showed essentially no loss of transmitted information. Three unidimensional features were extracted from spike patterns. Of those features, spike latency transmitted ϳ60% more information than that transmitted either by spike count or by a measure of latency dispersion. Information transmission by spike patterns recorded on single trials was substantially reduced compared with the information transmitted by averages of eight trials. In a comparison of averaged and nonaveraged responses, however, the information transmitted by latencies was reduced by only ϳ29%, whereas information transmitted by spike counts was reduced by 79%. Spike counts clearly are sensitive to sound-source location and could transmit information about sound-source locations. Nevertheless, the present results demonstrate that the timing of the first poststimulus spike carries a substantial amount, probably the majority, of the location-related information present in spike patterns. The results indicate that any complete model of the cortical representation of auditory space must incorporate the temporal characteristics of neuronal response patterns. I N T R O D U C T I O NThe spike patterns of auditory cortical neurons vary systematically as a function o...

Distinct Time Scales in Cortical Discrimination of Natural Sounds in Songbirds

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“…Surprisingly, the optimal temporal resolution we found at the cortical level was comparable to the optimal temporal resolution at the sensory periphery. Previous studies in auditory cortex have demonstrated the high degree of temporal precision in auditory cortical responses (DeWeese et al 2003;Elhilali et al 2004;Heil 1997;Heil and Irvine 1997), and the contribution of spike timing in the information transmitted by cortical neurons about time-varying stimuli (Lu and Wang 2004;) and sound location (Furukawa and Middlebrooks 2002). It is important to emphasize that the notion of the optimal temporal resolution for a detection or discrimination task is distinct from the temporal precision of neural responses, and these two quantities need not be the same for a neural code (Chichilnisky and Kalmar 2003).…”

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

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First-spike latency information in single neurons increases when referenced to population onset

“…However, most studies quantifying first-spike latency information assume that the brain has an independent reference for stimulus onset from which to extract latency. In the majority of situations, this independent onset reference does not exist; the need for a timing reference has caused some to question the ultimate feasibility of first-spike latency codes (8).A number of authors have suggested possible alternative latency measures (1,3,5,6), but few have actually compared the information contained in different onset references. Stecker and Middlebrooks (9) computed the information contained in the relative spike timing of pairs of simultaneously recorded neurons in auditory cortex, and Furukawa et al (10) compared the median errors from neural-network estimates of location with similar data.…”

“…A number of authors have suggested possible alternative latency measures (1,3,5,6), but few have actually compared the information contained in different onset references. Stecker and Middlebrooks (9) computed the information contained in the relative spike timing of pairs of simultaneously recorded neurons in auditory cortex, and Furukawa et al (10) compared the median errors from neural-network estimates of location with similar data.…”