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The Journal of Neuroscience, August 15, 2000, 20(16):6135-6143
Spatial-Temporal Distribution of Whisker-Evoked Activity in Rat Somatosensory Cortex and the Coding of Stimulus Location
Rasmus S. Petersen1 and Mathew E. Diamond1, 2 1 Cognitive Neuroscience Sector, International School for Advanced Studies, 34014 Trieste, Italy, and 2 Department of Biomedical Sciences and Technologies, University of Udine, 33100 Udine, Italy
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Rats use their facial vibrissae ("whiskers") to locate and identify objects. To learn about the neural coding of contact between whiskers and objects, we investigated the representation of single-vibrissa deflection by populations of cortical neurons. Microelectrode arrays, arranged in a geometric 10 × 10 grid, were inserted into the thalamo-recipient layers of "barrel cortex" (the vibrissal region of somatosensory cortex) in urethane-anesthetized rats, and neuronal activity across large sets of barrel-columns was measured. Typically, 5 msec after deflection of a whisker a 0.2 mm2 focus of activity emerged. It rapidly expanded, doubling in size by 7 msec, before retracting and disappearing 28-59 msec after stimulus onset. The total territory engaged by the stimulus ranged from 0.5 to 2.9 mm2 (2-11 barrels). Stimulus site dictated the domain of activity. To quantify the coding of whisker location, we applied the population d' measure of discriminability. Activity patterns elicited by two whiskers were highly discriminable at the initial cortical response; peak discriminability typically occurred within 16 msec of stimulus onset. To determine how widely information about stimulus location was distributed, we measured population d' while excluding response data from the on-center electrodes of the two tested whiskers. Response patterns remained discriminable, indicating that information about stimulus location was distributed across barrel cortex. Taken together, these results show that single-whisker deflections are represented in a multicolumn region constrained by barrel cortex map topography. The nature of this coding allows information about stimulus location to be coded extremely rapidly and unambiguously by one to two spikes per neuron.
Key words: cerebral cortex; electrophysiology; neurons/physiology; vibrissae; discriminability; barrel-column; population coding; multi-electrode
INTRODUCTION
The primary auditory, visual, and tactile cortical regions process sensory inputs in the framework of a large set of columnar, functional modules (Mountcastle, 1997
). Although decades of work have provided insights into how individual columns process and redistribute their afferent inputs (Fitzpatrick, 1996
The implication from these studies, then, is that the population of neurons participating in the representation of one whisker is distributed spatially across multiple barrel-columns. Although there have been attempts to "reconstruct" population responses on the basis of the synthesis of data from sequentially studied single neurons (Armstrong-James et al., 1992
Many of these concerns can be addressed because of recent advances in methodology. With the use of the Utah intracortical microelectrode array, neural events are collected simultaneously at 100 microelectrodes laid out in a geometric grid (Harris et al., 1999
it is thus well suited to the construction of stimulus-evoked cortical neural activity maps. Here we use the Utah array to reveal the temporal unfolding of barrel cortical neural activity maps in response to single-whisker deflections. We then apply the d' measure of signal detection theory to estimate the discriminability
MATERIALS AND METHODS
Subjects and experimental protocols. One advantage of using the 100-electrode recording array is that the large quantity of data collected in each subject reduces the number of experiments required. In the present study only three subjects were necessary to verify the consistency of all of the main results; see Table 1.
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Table 1. Consistency of principal results across subjects Details on experimental methodology are given in Rousche et al. (1999)
The array (Bionic Technologies, Salt Lake City, UT) consisted of a 10 × 10 grid of 1.0- or 1.5-mm-long electrodes with a 400 µm inter-electrode distance. Electrode array fabrication is described in Jones et al. (1992)
Array placement was examined in histological sections. At termination of the recording session the subjects were perfused with saline and 4% paraformaldehyde. After post-fixation in 20% sucrose, the cortex was removed, flattened, and frozen. The block of tissue was cut in 40 µm sections in the tangential plane and stained with cresyl violet.
Electrophysiological data acquisition. Individual whiskers were stimulated 3 mm from their base by a piezoelectric wafer (Morgan Matroc, Bedford, OH) that was controlled by a voltage pulse generator (A.M.P.I., Jerusalem, Israel). The stimulus, an up-down step function of 80 µm amplitude and 100 msec duration, was delivered at 1 Hz.
Initially, each macrovibrissa (A1-4, B1-4, C1-5, D1-5, E1-5,
,
,
, and
) was stimulated 50 times. The subset of whiskers for which the barrel-columns were penetrated by the array received a greater number of stimulus trials (279-500). Whiskers for which the barrel-columns lay at the edge of the array and for which the representations hence would have been sampled incompletely, were excluded from further analysis. The present results are based on the responses to 33 whiskers (rat r28: A1-2, B1-4, C1-4, D1-3, and E1-3; rat r30: C1-3, D1-3, and E1-2; rat r32: C1-4, D1-3, and E2-3).
The data acquisition system (Bionic Technologies) (Guillory and Normann, 1999
Analysis of neuronal responses. The first step was to form peristimulus time histograms (PSTHs) by using neural data collected at each electrode across all trials for a given stimulus site. For the purposes of illustration, neural data from all electrodes were used to form whole-array response maps (see Figs. 2B, 3, 6). However, for the quantification of cortical response parameters (see Figs. 4, 5, 7), only those electrodes at which the neural cluster gave a statistically significant response were included. Responding electrodes were identified by comparing the trial-by-trial poststimulus (0-100 msec) and prestimulus (
100 to 0 msec) multiunit spike counts, using the Wilcoxon signed ranks test (p < 0.01 accepted as a significant response).
On the basis of the observation that the principal whisker of a given barrel-column evokes the greatest response, we estimated the columnar location of each electrode (Ghazanfar and Nicolelis, 1999
For all responding electrodes the response onset latency was calculated by using a method similar to that of Maunsell and Gibson (1992)
To enable comparison with published data, we also estimated modal latencies, using the method of Armstrong-James and Fox (1987)
Discriminability of cortical population response patterns. To determine the discriminability among the neural responses to different whiskers, we adapted the signal detection measure d' (Green and Swets, 1966
, then:
This measure has been used to study how well single sensory neurons discriminate among relevant stimulus features (Tolhurst et al., 1983
(1) When more than one response variable is available, it is necessary to consider possible covariation among them across trials. If the responses to a given stimulus are statistically independent, then the population d' is simply the square root of the sum of the squared individual response d's (Green and Swets, 1966
where d'i is the discriminability at the ith response variable (electrode). Equation 2 also has been applied to sequentially recorded neurons, where no information about covariance was available (Zohary, 1992
(2)
where mx and my are mean response vectors across all electrodes, C is the matrix of covariances between pairs of electrodes, and T denotes matrix transposition. In the pattern recognition literature this measure of population d' is sometimes known as the Mahalanobis distance (see Duda and Hart, 1973
(3) In practice, means and covariances must be estimated from data. If there are electrodes at which neurons do not respond or respond very weakly, then the inverse covariance matrix can become subject to serious sampling error. In our case this problem was avoided in large part by repeating each stimulus many times (279-500 trials per whisker) and by restricting the analysis to electrodes for which the neurons yielded a significant response. Thus, if there were 10 responding electrodes in the 100-electrode array, then mx and my would be 10-dimensional, and C would be 10 × 10. In the few cases in which the covariance matrix remained singular, we computed discriminability in the subspace in which it was invertible (Metzner et al., 1998
(4) Given that C is a N×N matrix with rank R, then Q is the N×R matrix for which the columns are the R eigenvectors of C with non-zero eigenvalue, and
is the R×R diagonal matrix of corresponding eigenvalues.
Bias is another issue that arises when estimating d' from a finite set of data. Suppose that the identical stimulus is delivered across two sets of trials. Ideally, the discriminability between the two sets of responses would be zero. In practice, however, the difference between the two sample mean responses inevitably will be non-zero, resulting in a non-zero value of d'. In this light, it was important to estimate the chance d' value obtained by comparing response sets taken from the same stimulus. This was accomplished by randomly assigning the responses obtained for a given stimulus to two sets and estimating d' between these two sets. The procedure was repeated 10 times for each stimulus site, yielding estimates for the mean and SD of the chance d'. Thus, for each pair of stimulus sites a true d' estimate and two separate chance d' values were obtained (see Fig. 7A). Finally, the significance of the true d' was evaluated by computing z scores.
RESULTS
Cortical population response to a single whisker
The vibrissae of the snout are arranged in rows A-E, readily identifiable in all subjects (Fig. 1A), and neighborhood relations among whiskers are conserved in the local topographic relationships among the barrel-columns in contralateral primary somatosensory cortex (Woolsey and Van der Loos, 1970
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Figure 1. Sampling of the cortical vibrissal representation with a 10 × 10 electrode array. A, Disposition of the whiskers (shown as stubs) on the snout. Rows are labeled with letters A (dorsal) to E (ventral). B, Array position for rat r30 based on a photomicrograph of the preparation. Light gray shading is the dura mater exposed by the craniotomy. A 500 µm length of the electrodes is visible (shown in black), and the remaining 500 µm length (shown in white) is implanted in the tissue. C, Placement of the 10 × 10 microelectrode for rat r28. A barrel map was drawn from a nitric oxide synthetase-labeled tangential section (Valtschanoff et al., 1993
In each of the three experiments the neurons residing in ~20-30 cortical columns were recorded. This permitted us to generate maps representing the spatial distribution of the cortical population response as a function of stimulus site. Figure 2, A and B, illustrates the method by using rat r28 as an example. Vibrissa C1 was stimulated 279 times, and a PSTH with 2 msec bins was generated at each electrode for the interval from 40 msec before, until 40 msec after, stimulus onset. All 100 PSTHs are illustrated in Figure 2A. Those electrodes for which neurons gave the largest response are evident by the peak values in the PSTHs. Response magnitude evoked at each electrode was calculated as the average spike count for the 40 msec interval after stimulus onset minus the average spike count in the 40 msec prestimulus interval. In Figure 2B, these values have been plotted at the corresponding electrode positions, on a color scale, to create a "response map." The total number of responding electrodes was 14 (see Materials and Methods for statistical criteria).
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Figure 2. Cortical response to single whisker deflection. A, PSTH map for deflection of whisker C1 (r28); responding electrodes are enclosed by the red boundary. Orientation of the electrode sites is the same as in Figure 1C. B, Cortical response map on the basis of the PSTH data of A. For the purpose of illustration, a cubic interpolation was performed between electrodes. Activity is plotted on a logarithmic scale.
To learn about the unfolding of the cortical response over time, Figure 3 (top) illustrates neuronal activity in sequential 2 msec segments after upward deflection of whisker C2 in rat r32. In the time window 4-6 msec after stimulus onset, the cortical response emerged as a small central core focused on one electrode. In the time windows 8-10 and 10-12 msec after stimulus onset, the zone of activation expanded laterally to include an area of eight electrodes (1.28 mm2). Thereafter, the cortical activation
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Figure 3. Spatial and temporal features of the cortical response to a single whisker. Data were averaged across 466 stimulus trials delivered to whisker C2 in rat r32. Note the logarithmic scale.
To provide more detail concerning the spatial and temporal characteristics of the cortical response to stimulus onset, we generated population PSTHs. For each stimulus site the PSTHs at all responding electrodes were summated. The average of these 434 PSTHs from three rats is shown in Figure 4A. This composite PSTH reveals an extremely rapid response onset (5 msec) and an early peak in firing rate (8 msec), followed by a gradual dissipation of activity. Barrel cortex firing rate approached the prestimulus level within ~50 msec after stimulus onset. The contributions from on-center and off-center electrodes (see Materials and Methods for definitions) are shown separately in Figure 4B. The initial response can be attributed to on-center electrodes. The higher apparent background firing rate for the off-center PSTH is simply attributable to there being more such electrodes than on-center ones for the stimulation of any whisker.
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Figure 4. Characteristics of the cortical population response to whisker deflection. A, The composite PSTH was formed by summing 434 individual PSTHs across all responding electrodes for all stimuli in all rats. B, Composite PSTHs for on-center electrodes (solid line) and off-center electrodes (dotted line) are shown separately. The sum of these is the total PSTH of A. C, Histogram of total evoked spikes (across the entire array) per stimulus trial is plotted for the same data considered in A. D, For each stimulus site the number of responding electrodes was counted; the distribution of electrode counts is shown by using the bottom scale. The top scale indicates the corresponding cortical area, assuming each electrode to be representative of 0.16 mm2.
The average number of spikes summated across the neural clusters on all responding electrodes was evaluated for each stimulus site after the count of on-going prestimulus activity was subtracted, and the distribution of whole-array evoked spike counts is given in Figure 4C. The interquartile range (IQR) of the distribution is 3.0-8.1 spikes per stimulus trial.
How widely distributed was the response to single-whisker deflection? This was estimated by counting the total number of responding electrodes for each stimulus site. The distribution of electrode counts is given in Figure 4D. It is evident that the area activated by individual whiskers was highly variable, ranging from 3 to 18 electrodes. In every experiment the total set of responding electrodes formed a primarily contiguous field that overlaid the barrel field whisker region (see, for example, Fig. 1C). Nonresponding electrodes were almost always outside this field in sites lying beyond the whisker representation, e.g., in dysgranular zones (Chapin and Lin, 1990
From the spatial sampling density of the array we take each electrode to be representative of a 0.16 mm2 block of barrel cortex. The cortical territory activated by individual whiskers, then, was equivalent to 0.5-2.9 mm2. The number of distinct barrels activated was 2-11.
Examination of cortical response latency and response duration
The thalamocortical and intracortical pathways through which vibrissal sensory responses are generated has been a subject of debate (Simons and Carvell, 1989
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Figure 5. Emergence of the cortical population response. A, Onset latencies are mapped onto corresponding electrode positions (rat r28, stimulus site B1). Nonresponding electrodes are black. The electrode yielding the shortest latency response (6 msec) is indicated by the bullet. B, Distribution of latencies. The procedure of A was repeated for 33 whisker stimuli across three rats; a histogram of all latencies is shown. C, The solid line shows the expansion of activated cortical territory, averaged over all 33 stimuli. For this analysis an electrode was considered active at all times after its response onset, and cortical territory was derived from the number of electrodes. Error bars denote ±1 SD. The points indicate the rate of expansion of the active territory. D, The distribution of all response offsets for 33 stimuli.
For comparison with previously reported data (Armstrong-James and Fox, 1987
The onset latency analysis, coupled with the precise, regular spatial arrangement of the electrodes, allowed us to estimate the total cortical territory activated by a single-whisker stimulus as a function of poststimulus time. Similarly to Figure 4D, each electrode was taken to represent 0.16 mm2 of cortical tissue. Thus, as successive electrodes began to respond after whisker deflection, the active cortical zone grew. This time-dependent engagement of cortical territory is shown by the continuous line in Figure 5C, based on the average of all observations. Typically, 5 msec after whisker deflection a territory of 0.2 mm2 was active, corresponding to the principal barrel-column of the whisker. The activated area expanded very rapidly. By 7 msec, 0.5 mm2 was active; by 11 msec the active region had grown to 0.9 mm2. Because the area of a single barrel is ~0.1-0.2 mm2 (Rice, 1995
To determine the role of the number of trials on latency values, we repeated the analysis of onset latencies using randomly chosen sets of 50 trials. For each stimulus site we computed the difference in the latency across 279 and across 50 trials. The measured onset latency was slightly longer when only 50 trials were used (median increase, 1 msec; IQR, 0-2 msec). When only on-center electrodes were considered, the median increase was 0 msec (IQR, 0-1 msec). Thus, the small number of trials yields a later response onset at off-center electrodes.
The rapid time course of response onset suggests an anatomically direct thalamocortical route from one whisker to a relatively large area encompassing multiple barrel-columns. However, intracolumnar and intercolumnar circuits undoubtedly contribute to the subsequent processing of sensory information (Armstrong-James et al., 1993
Cortical response patterns and discriminability of stimulus site
Once the main features of the cortical response to a single whisker have been characterized, the next step is to determine how these features contribute to the coding of stimulus location. Cortical response patterns evoked by stimulation of whiskers C1, C2, C3, and C4 (rat r28) are shown in Figure 6. One whisker activated a cortical field corresponding to the on-center barrel-column and a set of surrounding barrel-columns. The location of cortical activity was related to stimulus site, as one would predict on the basis of the well known barrel map (Woolsey and Van der Loos, 1970
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Figure 6. Projection of whiskers C1-C4 onto barrel cortex (rat r28). Response maps were generated from the spike count 0-100 msec poststimulus, as in Figure 2B.
To answer these questions, it was necessary to quantify how reliably two stimuli could be discriminated on the basis of the neural responses. One strategy commonly applied to electrophysiological signals recorded at single electrodes is the d' measure of signal detection theory (Tolhurst et al., 1983
Using the data illustrated in Figure 6, we calculated d' for one pair of whisker-evoked patterns (Fig. 7A). Figure 7A (circles, top trace) shows the time course of discriminability for C2 versus C3 in r28 on the basis of cumulative responses in 4 msec steps: i.e., 0-4, 0-8, 0-12 msec, etc. The bottom trace is the expected chance d' (error bars denote ±1 SD; see Materials and Methods). At 4 msec poststimulus the discriminability was at chance level; by 8 msec it was above chance. At 16 msec after stimulus onset it had reached its maximum value of 4, after which discriminability declined. Figure 7B shows d' averaged over all 184 stimulus pairs, together with the SD. The median time at which d' reached its peak was 16 msec; the IQR was 16-28 msec. It was very common, therefore, for spikes occurring >16 msec after stimulus onset to contribute no information about stimulus location (on average, 32% of evoked spikes occurred later than 16 msec).
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Figure 7. Discriminability between cortical response patterns. A, Population d' was estimated for the cortical response to C2 versus C3 in rat r28 in cumulative time bins (top trace). The estimated chance d' is shown also (bottom trace). The error bars are ±1 SD of the chance d'. B, Average population d' across all pairs of stimuli in three rats. The error bars are ±1 SD. C, The population d' was estimated for the same stimulus pair shown in A, but we used only on-center electrodes (squares) or only off-center electrodes (diamonds). D, Average population d' (circles) is compared with the average when only on-center electrodes are used (squares) and when only off-center electrodes are used (diamonds).
If the representation of single whiskers was strictly topographic, d' would depend exclusively on activity in the two barrel-columns topographically matched to the two stimulated whiskers. If, on the other hand, the representation was distributed, there also would be a significant contribution from nonprincipal barrel-columns. To distinguish between these possibilities, we took on-center electrodes to correspond to principal barrel-columns. Then, we compared d' derived from all responding electrodes (Fig. 7A,B) with that derived only from off-center electrodes (Fig. 7C,D). Figure 7C shows the result for the same data used in Figure 7A, but with only off-center electrodes (diamonds). The peak discriminability decreased from 4.0 to 2.4 but remained well above chance. Indeed, for 183 of 184 stimulus pairs the peak discriminability exceeded the chance level by at least 4 SD even after the removal of on-center electrodes. This means that the activity present at off-center barrel-columns as a group remains capable of supporting the discrimination between this pair of whiskers. On average (Fig. 7D), by excluding on-center electrodes, peak discriminability decreased from 4.3 (circles) to 1.9 (diamonds), and the peak was delayed (30 msec as opposed to 16 msec poststimulus).
Perhaps a more ecologically relevant question is whether activity at off-center electrodes actually improves the reliability of stimulus localization. To find out, we repeated the analysis using only on-center electrodes. On-center electrodes alone supported good discriminability (squares in Fig. 7C,D), but peak d' was, on average, 10% lower than when off-center channels also were included (compare circles with squares in Fig. 7D). This comparison also indicated that the initial rapid rise in discriminability 0-8 msec after stimulus onset was attributable to on-center electrodes. The spread of single-whisker activity to off-center barrel-columns thus provided a modest increase in reliability of the coding for the stimulus site.
DISCUSSION
Principal findings
By using a large array of 100 closely spaced electrodes covering 13 mm2, we recorded simultaneously from a large portion of whisker-related SI. Previous investigations concerning the spatial distribution of activity either have attempted to reconstruct the cortical response from sequentially recorded single units (Armstrong-James et al., 1992
To explore the population coding of stimulus site, we examined whisker discriminability by using the d' measure of signal detection theory. The relevant information begins to be present in somatosensory cortex some 5 msec after deflection of the whisker, allowing an appropriate behavior to be initiated rapidly. Discriminability between pairs of whisker-evoked response patterns was highly robust as early as 8 msec after stimulus onset and was maximal at 16 msec. It is the early cortical response, therefore, that supports discriminability. Off-center barrel-columns do contribute to stimulus discriminability, but much less, and more slowly, than do on-center barrel-columns. Discriminability is accounted for in large part by on-center barrel-columns, but reliability of the discrimination is improved by ~10% as a result of the distribution of activity across multiple barrel-columns.
Cortical response patterns and the underlying circuitry
Single-whisker deflection activated 2-11 barrel-columns lying within a cortical territory of 0.5-2.9 mm2. The average initial activation encompassed 0.2 mm2 (one barrel-column) at 5 msec and expanded extremely rapidly. In 50% of cases at least three different barrel-columns were activated within 10 msec of stimulus onset.
Armstrong-James and colleagues (Armstrong-James and Fox, 1987
However, there is a key difference regarding results for nonprincipal whisker stimulation. Armstrong-James and Fox (1987)
In contrast to some earlier claims, therefore, it seems that there is a direct, thalamic route by which surround-receptive fields are generated in the middle cortical layers
Intercolumnar cortical pathways
The cortical representation of single whiskers
The activity patterns described in this paper probably do not constitute the unique manner in which single-whisker information is represented across barrel cortex. Several factors influence the cortical response to whisker deflection. The type and dosage of anesthetic have a complex relationship with the size of cortical response patterns (Chapin and Lin, 1984
Even if our data reflect only one of many possible operating modes of the available sensory system circuitry, the nature of the whisker representation uncovered here seems to agree with evidence from naturally behaving rats. The same fundamental whisker-to-cortex projection we have shown
Speed of whisker processing
We found that the peak discriminability between whisker response patterns occurred 16 msec after deflection, on average. Because only a few neurons per barrel-column were sampled and because only information in the time-varying firing rate was considered, this should be considered a conservative estimate. It is likely therefore that, in layers III-IV, information about stimulation site is carried by the spatially focused early cortical response rather than the more diffuse late response. For the d' measure, those spikes occurring later than the time of peak d' can be regarded as contributing only "noise" to the discrimination of stimulus location. In our data set, therefore, activity recorded later than 16 msec poststimulus (32% of all spikes) was noise. During a behavioral task such as gap crossing, where differences in the sensory signal evoked by different whiskers have real behavioral significance (Harris et al., 1999
Within such a short time interval any given cortical neuron will have fired at most one to two spikes. The same conclusion
FOOTNOTES Received Oct. 22, 1999; revised May 8, 2000; accepted May 11, 2000.
This work was supported by National Institutes of Health Grant NS32647, Telethon Foundation Grant 984, and Ministero dell'Universite della Ricerca Scientifica e Technologica. We thank T. Celikel for assistance with some experiments and S. Giannotta for technical assistance. We are grateful to W. Bialek, P. Dayan, L. Martignon, M. Shukla, and A. Treves for useful discussions.
Correspondence should be addressed to Dr. Mathew E. Diamond, Cognitive Neuroscience Sector, International School for Advanced Studies, Via Beirut, 2-4, 34014 Trieste, Italy. E-mail: diamond{at}sissa.it.
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