Rasmus S. Petersen

The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex

Although the timing of single spikes is known to code for time-varying features of a sensory stimulus, it remains unclear whether time is also exploited in the neuronal coding of the spatial structure of the environment, where nontemporal stimulus features are fundamental. This report demonstrates that, in the whisker representation of rat cortex, precise spike timing of single neurons increases the information transmitted about stimulus location by 44%, compared to that transmitted only by the total number of spikes. Crucial to this code is the timing of the first spike after whisker movement. Complex, single neuron spike patterns play a smaller, synergistic role. Timing permits very few spikes to transmit high quantities of information about a behaviorally significant, spatial stimulus.

Population Coding of Stimulus Location in Rat Somatosensory Cortex

This study explores the nature of population coding in sensory cortex by applying information theoretic analyses to neuron pairs recorded simultaneously from rat barrel cortex. We quantified the roles of individual spikes and spike patterns in encoding whisker stimulus location. 82%-85% of the total information was contained in the timing of individual spikes: first spike time was particularly crucial. Spike patterns within neurons accounted for the remaining 15%-18%. Neuron pairs located in the same barrel column coded redundantly, whereas pairs in neighboring barrel columns coded independently. The barrel cortical population code for stimulus location appears to be the time of single neurons first poststimulus spikes-a fast, robust coding mechanism that does not rely on synergy in crossneuronal spike patterns.

Encoding of whisker vibration by rat barrel cortex neurons: implications for texture discrimination.

Rats, using their whiskers, have excellent capabilities in texture discrimination. What is the representation of texture in rat somatosensory cortex? We hypothesize that as rats “whisk” over a surface, the spatial frequency of a grooved or pebbled texture is converted to a temporal frequency of whisker vibration. Surface features such as groove depth or grain size modulate the amplitude of this vibration. Validation of the hypothesis depends on showing that vibration parameters have distinct neuronal representations in cortex. To test this, we delivered sinusoidal vibrations to the whisker shaft and analyzed cortical neuronal activity. Seven amplitudes and seven frequencies were combined to construct 49 stimuli while recording activity through a 10 × 10 microelectrode array inserted into the middle layers of barrel cortex. We find that cortical neurons do not explicitly encode vibration frequency (f) or amplitude (A) by any coding measure (average spike counts over different time windows, spike timing patterns in the peristimulus time histograms or in autocorrelograms). Instead, neurons explicitly encode the product of frequency and amplitude, which is proportional to the mean speed of the vibration. The quantity Af is an invariant because neuronal response encodes this feature independently of the values of the individual terms A and f. This was true across a wide time scale of firing rate measurements, from 5 to 500 msec. We conclude that vibration kinetics are rapidly and reliably encoded in the firing rate of cortical ensembles. Therefore, the cortical representation of vibration speed could underlie texture discrimination.

Population coding in somatosensory cortex.

Computational analyses have begun to elucidate which components of somatosensory cortical population activity may encode basic stimulus features. Recent results from rat barrel cortex suggest that the essence of this code is not synergistic spike patterns, but rather the precise timing of single neurons first post-stimulus spikes. This may form the basis for a fast, robust population code.

Examination of the spatial and temporal distribution of sensory cortical activity using a 100-electrode array

This paper introduces improved techniques for multichannel extracellular electrophysiological recordings of neurons distributed across a single layer of topographically mapped cortex. We describe the electrode array, the surgical implant techniques, and the procedures for data collection and analysis. Neural events are acquired through an array of 25 or 100 microelectrodes with a 400-microm inter-electrode spacing. One advantage of the new methodology is that implantation is achieved through transdural penetration, thereby reducing the disruption of the cortical tissue. The overall cortical territory sampled by the 25-electrode array is 1.6 x 1.6 mm (2.56 mm2) and by the 100-electrode array 3.6 x 3.6 mm (12.96 mm2). Using a recording system with 100 channels available, neural activity is simultaneously acquired on all electrodes, amplified, digitized, and stored on computer. In our data, average peak-to-peak signal/noise ratio was 11.5 and off-line waveform analysis typically allowed the separation of at least one well-discriminated single-unit per channel. The reported technique permits analysis of cortical function with high temporal and spatial resolution. We use the technique to create an image of neural activity distributed across the whisker representation of rat somatosensory (barrel) cortex.

Learning through maps: Functional significance of topographic organization in primary sensory cortex

The presence of maps in sensory cortex is a hallmark of the mammalian nervous system, but the functional significance of topographic organization has been called into question by physiological studies claiming that patterns of neural behavioral activity transcend topographic boundaries. This paper discusses recent behavioral and physiological studies suggesting that, when animals or human subjects learn perceptual tasks, the neural modifications associated with the learning are distributed according to the spatial arrangement of the primary sensory cortical map. Topographical cortical representations of sensory events, therefore, appear to constitute a true structural framework for information processing and plasticity.

The Cortical Distribution of Sensory Memories

Recent investigations are allowing precise statements to be made about where in the cortex sensory memories are stored and retrieved. After highlighting new work that has refined the long-recognized contributions of frontal and temporal association areas, this review turned to sensory cortex and suggested that its role in the storage of sensory information and in the retrieval of perceptual memories is not qualitatively different from that played by “later” association areas. In particular, we presented evidence that neuronal activity in sensory cortex contributes to remembering the sensory features of a stimulus. Studies in species as different as humans and rats show that learned recognition of elemental stimulus features can be strictly localized in a way that is best accounted for by information storage within the framework of sensory cortical maps. Finally, electrophysiological studies in monkeys have shown that learning to recognize a stimulus is based on distinct changes in the patterns of neuronal activity in sensory cortex. Thus, each functional region of cortex appears to carry out the dual functions of information processing and information storage. Storage and retrieval involve the very populations of cortical neurons that explicitly encode the relevant information, ensuring that the stored and recalled information is of comparable quality to the information present during on-line processing.

The role of individual spikes and spike patterns in population coding of stimulus location in rat somatosensory cortex

This report addresses the nature of population coding in sensory cortex by applying information theoretic analysis to data recorded simultaneously from neuron pairs located in primary somatosensory cortex of anaesthetised rats. We studied how cortical spike trains code for the location of a whisker stimulus on the rats snout. We found that substantially more information was conveyed by 10 ms precision spike timing compared with that conveyed by the number of spikes counted over a 40 ms response interval. Most of this information was accounted for by the timing of individual spikes. In particular, it was the first post-stimulus spikes that were crucial. Spike patterns within individual cells played a smaller role; spike patterns across cells were negligible. This pattern of results was robust both to the exact nature of the stimulus set and to the precision at which spikes were binned.

A critical assessment of different measures of the information carried by correlated neuronal firing

Information theoretic measures have been proposed as a quantitative framework to clarify the role of correlated neuronal activity in the brain. In this paper we review some recent methods that allow precise assessments of the role of correlation in stimulus coding and decoding by the nervous system. We present new results that make explicit links between types of encoding and decoding mechanisms based on correlations. We illustrate the concepts by showing that the spike trains of pairs of neurons in rat somatosensory cortex can be decoded almost perfectly without including knowledge of correlation in the read-out model, although in this neural system correlations between spike times contribute appreciably to stimulus encoding.

Investigations into the organization of information in sensory cortex

One might take the exploration of sensory cortex in the first decades of the last century as the opening chapter of modern neuroscience. The combined approaches of (i) measuring effects of restricted ablation on functional capacities, both in the clinic and the laboratory, together with (ii) anatomical investigations of cortical lamination, arealization, and connectivity, and (iii) the early physiological probing of sensory representations, led to a fundamental body of knowledge that remains relevant to this day. In our time, there can be little doubt that its organization as a mosaic of columnar modules is the pervasive functional property of mammalian sensory cortex [Brain 120 (1997) 701]. If one accepts the assertion that columns and maps must improve the functioning of the brain (why else would they be the very hallmark of neocortex?), then the inevitable question is: exactly what advantages do they permit? In this review of our recent presentation at the workshop on Homeostasis, plasticity and learning at the Institut Henri Poincaré, we will outline a systematic approach to investigating the role of modular, map-like cortical organization in the processing of sensory information. We survey current evidence concerning the functional significance of cortical maps and modules, arguing that sensory cortex is involved not solely in the online processing of afferent data, but also in the storage and retrieval of information. We also show that the topographic framework of primary sensory cortex renders the encoding of sensory information efficient, fast and reliable.