Search PubMed⌕ Search

Biomedical subjects

Mathew E Diamond

Publications and source records attributed to Mathew E Diamond.

17 recordsLinked to original sources

Factors affecting frequency discrimination of vibrotactile stimuli: implications for cortical encoding.

BACKGROUND: Measuring perceptual judgments about stimuli while manipulating their physical characteristics can uncover the neural algorithms underlying sensory processing. We carried out psychophysical experiments to examine how humans discriminate vibrotactile stimuli. METHODOLOGY/PRINCIPAL FINDINGS: Subjects compared the frequencies of two sinusoidal vibrations applied sequentially to one fingertip. Performance was reduced when (1) the root mean square velocity (or energy) of the vibrations was equated by adjusting their amplitudes, and (2) the vibrations were noisy (their temporal structure was irregular). These effects were super-additive when subjects compared noisy vibrations that had equal velocity, indicating that frequency judgments became more dependent on the vibrations' temporal structure when differential information about velocity was eliminated. To investigate which areas of the somatosensory system use information about velocity and temporal structure, we required subjects to compare vibrations applied sequentially to opposite hands. This paradigm exploits the fact that tactile input to neurons at early levels (e.g., the primary somatosensory cortex, SI) is largely confined to the contralateral side of the body, so these neurons are less able to contribute to vibration comparisons between hands. The subjects' performance was still sensitive to differences in vibration velocity, but became less sensitive to noise. CONCLUSIONS/SIGNIFICANCE: We conclude that vibration frequency is represented in different ways by different mechanisms distributed across multiple cortical regions. Which mechanisms support the "readout" of frequency varies according to the information present in the vibration. Overall, the present findings are consistent with a model in which information about vibration velocity is coded in regions beyond SI. While adaptive processes within SI also contribute to the representation of frequency, this adaptation is influenced by the temporal regularity of the vibration.

Adolescent↗

Deciphering the spike train of a sensory neuron: counts and temporal patterns in the rat whisker pathway.

Rats achieve remarkable texture discriminations by sweeping their facial whiskers along surfaces. This work explores how neurons at two levels of the sensory pathway, trigeminal ganglion and barrel cortex, carry information about such stimuli. We identified two biologically plausible coding mechanisms, spike counts and patterns, and used "mutual information" to quantify how reliably neurons in anesthetized rats reported texture when "decoded" according to these candidate mechanisms. For discriminations between surfaces of different coarseness, spike counts could be decoded reliably and rapidly (within 30 ms after stimulus onset in cortex). Information increased as responses were considered as spike patterns with progressively finer temporal precision. At highest temporal resolution (spike sequences across six bins of 4 ms), the quantity of "information" in patterns rose 150% for ganglion neurons and 110% for cortical neurons above that in spike counts. In some cases, patterns permitted discriminations not supported by spike counts alone.

Action Potentials↗

Active sensation: insights from the rodent vibrissa sensorimotor system.

Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rat's head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.

Action Potentials↗

Neuronal encoding of natural stimuli: the rat tactile system.

A major challenge of sensory systems neuroscience is to quantify the brain activity underlying perceptual experiences and to explain this activity as the outcome of elemental neuronal response properties. One strategy is to measure variations in neuronal response in relation to controlled variations in an artificial stimulus. The limitation is that the stimuli scarcely resemble those which the sensory system has evolved to process-natural, behaviourally relevant stimuli. A more recent strategy is to measure neuronal responses during presentation of natural stimuli, but such experiments have failed to predict the observed responses according to the fundamental properties of neurons. In the work described here, we focus on tactile sensation in rats, and try to bridge the gap between neurons' responses to natural stimuli and their responses to controlled, artificial stimuli. We focus on texture, a submodality in which the rat whisker sensory system excels. Because the physical characteristics of texture stimuli have not yet been studied, the first set of experiments measures textures from the whiskers' point of view. The second set of experiments describes neurons' responses to textures. The third set of experiments computes kernels (estimates of the extracted stimulus features) of sensory neurons using white noise and then tries to account for natural texture responses according to these kernels. These investigations suggest ways of using natural stimuli to assemble a more complete picture of the neuronal basis of tactile sensation.

Afferent Pathways↗

Texture signals in whisker vibrations.

Rodents excel in making texture judgments by sweeping their whiskers across a surface. Here we aimed to identify the signals present in whisker vibrations that give rise to such fine sensory discriminations. First, we used sensors to capture vibration signals in metal whiskers during active whisking of an artificial system and in natural whiskers during whisking of rats in vivo. Then we developed a classification algorithm that successfully matched the vibration frequency spectra of single trials to the texture that induced it. For artificial whiskers, the algorithm correctly identified one texture of eight alternatives on 40% of trials; for in vivo natural whiskers, the algorithm correctly identified one texture of five alternatives on 80% of trials. Finally, we asked which were the key discriminative features of the vibration spectra. Under both artificial and natural conditions, the combination of two features accounted for most of the information: The modulation power-the power of the part of the whisker movement representing the modulation due to the texture surface-increased with the coarseness of the texture; the modulation centroid-a measure related to the center of gravity within the power spectrum-decreased with the coarseness of the texture. Indeed, restricting the signal to these two parameters led to performance three-fourths as high as the full spectra. Because earlier work showed that modulation power and centroid are directly related to neuronal responses in the whisker pathway, we conclude that the biological system optimally extracts vibration features to permit texture classification.

Action Potentials↗

Neuronal encoding of texture in the whisker sensory pathway.

A major challenge of sensory systems neuroscience is to quantify brain activity underlying perceptual experiences and to explain this activity as the outcome of elemental neuronal response properties. Rats make extremely fine discriminations of texture by "whisking" their vibrissae across an object's surface, yet the neuronal coding underlying texture sensations remains unknown. Measuring whisker vibrations during active whisking across surfaces, we found that each texture results in a unique "kinetic signature" defined by the temporal profile of whisker velocity. We presented these texture-induced vibrations as stimuli while recording responses of first-order sensory neurons and neurons in the whisker area of cerebral cortex. Each texture is encoded by a distinctive, temporally precise firing pattern. To look for the neuronal coding properties that give rise to texture-specific firing patterns, we delivered horizontal and vertical whisker movements that varied randomly in time ("white noise") and found that the response probabilities of first-order neurons and cortical neurons vary systematically according to whisker speed and direction. We applied the velocity-tuned spike probabilities derived from white noise to the sequence of velocity features in the texture to construct a simulated texture response. The close match between the simulated and real responses indicates that texture coding originates in the selectivity of neurons to elemental kinetic events.

Animals↗

Rapid fluctuations in rat barrel cortex plasticity.

Neuronal populations in the sensory cortex exhibit fluctuations in excitability, and the present experiments tested the hypothesis that these variations coincide with peaks and troughs in cortical modifiability. The activity of multiunit neuronal clusters under light urethane anesthesia was recorded through 100-microelectrode arrays implanted in the infragranular layers of rat barrel cortex. Spontaneous activity was characterized by "bursts" of spikes, synchronized across the barrel cortex. This allowed activity at one selected electrode to be taken as a reliable monitor of widespread cortical bursts. We used spikes at the selected electrode to trigger stimulation of two pairs of whiskers during a 50 min conditioning procedure: (1) for the "burst-conditioned" whisker pair, each stimulus was delivered 1 msec after the triggering spike, activating cortex coincident with the burst; and (2) for the "interburst-conditioned" whisker pair, each stimulus was delivered 300 msec after the triggering spike, activating cortex during the trough between bursts. The cross-correlation between cortical neurons in the pairs of columns matching the stimulated whisker pairs was estimated after the termination of the conditioning procedure. Conditioning produced a twofold increase in the degree of co-firing between infragranular neurons in columns receiving burst-conditioned costimulation but no significant change in connectivity between infragranular neurons in columns receiving interburst-conditioned costimulation, although the two pairs of columns received an equal number of sensory inputs. These findings suggest that the strength of co-activity between columns in the barrel cortex can be modified by sensory input patterns during discrete, intermittent intervals time-locked to bursts.

Action Potentials↗

Whisker vibration information carried by rat barrel cortex neurons.

Rats can make extremely fine texture discriminations by "whisking" their vibrissa across the surface of an object. We have investigated one hypothesis for the neuronal basis of texture representation by measuring how clusters of neurons in the barrel cortex of anesthetized rats encode the kinetic features of sinusoidal whisker vibrations. Mutual information analyses of spike counts led to a number of findings. Information about vibration kinetics became available as early as 6 msec after stimulus onset and reached a peak at approximately 20-30 msec. Vibration speed, proportional to the product of vibration amplitude (A) and frequency (f), was the kinetic property most reliably reported by cortical neurons. Indeed, by measuring information when the complete stimulus set was collapsed into feature-defined groups, we found that neurons reduced the dimensionality of the stimulus from two features (A, f) to a single feature, the product Af. Moreover, because different neurons encode stimuli in the same manner, information loss was negligible even when the activity of separate neuronal clusters was pooled. This suggests a decoding scheme whereby target neurons could capture all available information simply by summating the signals from separate barrel cortex neurons. These results indicate that neuronal population activity provides sufficient information to allow nearly perfect discrimination of two vibrations, based on their deflection speeds, within a time scale comparable with that of a single whisking motion across a surface.

Animals↗

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 x 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.

Action Potentials↗

Effect of developmental sensory and motor deprivation on the functional organization of adult rat somatosensory cortex.

Most sensory systems are active, in the sense that the animal performs specific motor actions in order to collect information of interest-signals are not merely passively received. We, therefore, expect cortical development to depend not only correct sensory experience, but also on correct motor experience. In this study, we used the rat whisker system as a model to compare the importance of these factors. In one group of animals, we trimmed all whiskers starting from post-natal day 8 (P8). In a second group, we left the whiskers intact, but prevented "whisking" by sectioning the facial (VIIth cranial) nerve on P8. The first group had severely disrupted sensory experience but normal motor patterns ("whisker-cut" rats); the second group had normal sensory pathways within which temporal activity patterns were disrupted by motor impairment ("nerve-cut" rats). When they reached 3 months of age, we recorded multi-unit responses from the infragranular layers of primary somatosensory cortex in response to deflection of either single whiskers or pairs of whiskers in order to compare these two groups to a third group of rats that had normal sensory and motor experience. Cortical topographic organization was unaltered in whisker- and nerve-cut rats. Whisker-cut rats showed a smaller than normal difference between the response magnitudes for the principal and surrounding whiskers, as well as stronger than normal interactions between co-active whisker inputs. Responses in nerve-cut rats were nearly indistinguishable from those in normal animals. Thus, unexpectedly, neither pure sensory nor sensorimotor deprivation caused gross functional disruption of SI according to our measures. It appears that abnormal sensory experience leads to alterations in the fine-tuning of cortical properties, but cortex is unexpectedly resistant to the effects of abnormal sensory and sensorimotor experience.

Action Potentials↗

Decoding neuronal population activity in rat somatosensory cortex: role of columnar organization.

The present study asks in what way the activity of a neuronal population responding to a sensory stimulus could be most efficiently decoded, or 'read off', by the target neurons. A simple solution to this problem has been proposed - pooling the activity of responding neurons. However, pooling can be inefficient if sensory information is encoded by the 'label' of each neuron firing a spike. We have tested the efficiency of pooling by quantifying the extent to which information about a sensory stimulus is diminished when the identity of the individual neurons is lost by pooling. Analyzing the response of small groups of neurons in rat barrel cortex to single-whisker deflection, we found that pooling neurons within the same column is efficient for representing stimulus position; it causes a loss of only 1% of the information about whether the principal whisker was stimulated, and a loss of 5-12% of the finer information about which of nine possible whiskers (the principal and its neighbors) was stimulated. Cross-column pooling led to larger information losses, in the range of 25-55%. Thus, to decode stimulus position from the discharge of barrel cortex populations, 'downstream' neurons could pool the activity arising from neurons of the same column, while maintaining the activity arising from neurons of separate columns at least partially segregated. Since such parcellation is present in some of the projections from barrel cortex, these findings suggest that columnar organization of barrel cortex serves to facilitate decoding of the location of the stimulated whisker.

Action Potentials↗

Transient storage of a tactile memory trace in primary somatosensory cortex.

Working memory is known to involve prefrontal cortex and posterior regions of association cortex (e.g., the inferior temporal lobes). Here, we investigate the potential role of primary somatosensory cortex (SI) in a working memory task with tactile stimuli. Subjects were required to compare the frequencies of two vibrations separated by a retention interval of 1500 msec. Their performance was significantly disrupted when we delivered a pulse of transcranial magnetic stimulation (TMS) to the contralateral SI early (300 or 600 msec) in the retention interval. TMS did not affect tactile working memory if delivered to contralateral SI late in the retention interval (at 900 or 1200 msec), nor did TMS affect performance if delivered to the ipsilateral SI at any time point. Primary sensory cortex thus seems to act not only as a center for on-line sensory processing but also as a transient storage site for information that contributes to working memory.

Adult↗

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 neuron's first post-stimulus spikes. This may form the basis for a fast, robust population code.

Action Potentials↗

Somatosensory cortical neuronal population activity across states of anaesthesia.

Experiments were carried out to learn about changes in sensory cortical processing associated with different levels of anaesthesia. Traditionally this question has been addressed by studying single neurons. Because state changes are likely to influence the relationships between neurons, the present experiments were undertaken to investigate the spatial and temporal firing patterns distributed across cortex. Using 5 x 5 or 10 x 10 microelectrode arrays, spontaneous and stimulus-evoked activity of multineuron clusters was recorded from rat somatosensory 'barrel' cortex (the whisker representation) during a light surgical stage of urethane anaesthesia, and after two supplemental doses of urethane which led to intermediate and deep levels of anaesthesia. At all depths of anaesthesia, spontaneously occurring action potentials at a single electrode tended to be clustered into 'bursts.' With increasing anaesthetic depth, bursts became more prominent and rhythmic, and increasingly synchronized between cortical barrel-columns. Burst frequency decreased and fewer spikes occurred outside bursts, leading to a decrease in the overall spontaneous firing rate. The cortical territory engaged by individual whiskers contracted with increasing depth of anaesthesia, leading to the spatial segregation of whisker representations. At all stages of anaesthesia, whisker stimulation produced the maximal cortical response when delivered close to burst onset. These observations show that ongoing spontaneous activity modulates sensory response properties and makes peripheral tactile information accessible to a cortical territory whose size is determined by the phase of burst cycle. The possible significance of the cyclic cortical responsiveness encountered during urethane anaesthesia to cortical processing in awake rats is considered.

Action Potentials↗

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.

Animals↗

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 rat's 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.

Action Potentials↗

Redundancy and synergy arising from pairwise correlations in neuronal ensembles.

Multielectrode arrays allow recording of the activity of many single neurons, from which correlations can be calculated. The functional roles of correlations can be revealed by measures of the information conveyed by neuronal activity; a simple formula has been shown to discriminate the information transmitted by individual spikes from the positive or negative contributions due to correlations (Panzeri et al., 1999). Here, this analysis, previously applied to recordings from small ensembles, is developed further by considering a model of a large ensemble, in which correlations among the signal and noise components of neuronal firing are small in absolute value and entirely random in origin. Even such small random correlations are shown to lead to large possible synergy or redundancy, whenever the time window for extracting information from neuronal firing extends to the order of the mean interspike interval. In addition, a sample of recordings from rat barrel cortex illustrates the mean time window at which such "corrections" dominate when correlations are, as often in the real brain, neither random nor small. The presence of this kind of correlations for a large ensemble of cells restricts further the time of validity of the expansion.

Action Potentials↗