Adaptation and Temporal Decorrelation by Single Neurons in the Primary Visual Cortex

2003 ◽  
Vol 89 (6) ◽  
pp. 3279-3293 ◽  
Author(s):  
Xiao-Jing Wang ◽  
Yinghui Liu ◽  
Maria V. Sanchez-Vives ◽  
David A. McCormick

Limiting redundancy in the real-world sensory inputs is of obvious benefit for efficient neural coding, but little is known about how this may be accomplished by biophysical neural mechanisms. One possible cellular mechanism is through adaptation to relatively constant inputs. Recent investigations in primary visual (V1) cortical neurons have demonstrated that adaptation to prolonged changes in stimulus contrast is mediated in part through intrinsic ionic currents, a Ca2+-activated K+ current ( IKCa) and especially a Na+-activated K+ current ( IKNa). The present study was designed to test the hypothesis that the activation of adaptation ionic currents may provide a cellular mechanism for temporal decorrelation in V1. A conductance-based neuron model was simulated, which included an IKCa and an IKNa. We show that the model neuron reproduces the adaptive behavior of V1 neurons in response to high contrast inputs. When the stimulus is stochastic with 1/ f 2 or 1/ f-type temporal correlations, these autocorrelations are greatly reduced in the output spike train of the model neuron. The IKCa is effective at reducing positive temporal correlations at approximately 100-ms time scale, while a slower adaptation mediated by IKNa is effective in reducing temporal correlations over the range of 1–20 s. Intracellular injection of stochastic currents into layer 2/3 and 4 (pyramidal and stellate) neurons in ferret primary visual cortical slices revealed neuronal responses that exhibited temporal decorrelation in similarity with the model. Enhancing the slow afterhyperpolarization resulted in a strengthening of the decorrelation effect. These results demonstrate the intrinsic membrane properties of neocortical neurons provide a mechanism for decorrelation of sensory inputs.

1991 ◽  
Vol 66 (4) ◽  
pp. 1156-1165 ◽  
Author(s):  
V. L. Smith-Swintosky ◽  
C. R. Plata-Salaman ◽  
T. R. Scott

1. Extracellular action potentials were recorded from 50 single neurons in the insular-opercular cortex of two alert cynomolgus monkeys during gustatory stimulation of the tongue and palate. 2. Sixteen stimuli, including salts, sugars, acids, alkaloids, monosodium glutamate, and aspartame, were chosen to represent a wide range of taste qualities. Concentrations were selected to elicit a moderate gustatory response, as determined by reference to previous electrophysiological data or to the human psychophysical literature. 3. The cortical region over which taste-evoked activity could be recorded included the frontal operculum and anterior insula, an area of approximately 75 mm3. Taste-responsive cells constituted 50 (2.7%) of the 1,863 neurons tested. Nongustatory cells responded to mouth movement (20.7%), somatosensory stimulation of the tongue (9.6%), stimulus approach or anticipation (1.7%), and tongue extension (0.6%). The sensitivities of 64.6% of these cortical neurons could not be identified by our stimulation techniques. 4. Taste cells had low spontaneous activity levels (3.7 +/- 3.0 spikes/s, mean +/- SD) and showed little inhibition. They were moderately broadly tuned, with a mean entropy coefficient of 0.76 +/- 0.17. Excitatory responses were typically not robust. 5. Hierarchical cluster analysis was used to determine whether neurons could be divided into discrete types, as defined by their response profiles to the entire stimulus array. There was an apparent division of response profiles into four general categories, with primary sensitivities to sodium (n = 18), glucose (n = 15), quinine (n = 12), and acid (n = 5). However, these categories were not statistically independent. Therefore the notion of functionally distinct neuron types was not supported by an analysis of the distribution of response profiles. It was the case, however, that neurons in the sodium category could be distinguished from other neurons by their relative specificity. 6. The similarity among the taste qualities represented by this stimulus array was assessed by calculating correlations between the activity profiles they elicited from these 50 neurons. The results generally confirmed expectations derived from human psychophysical studies. In a multidimensional representation of stimulus similarity, there were groups that contained acids, sodium salts, and chemicals that humans label bitter and sweet. 7. The small proportion of insular-opercular neurons that are taste sensitive and the low discharge rates that taste stimuli are able to evoke from them suggest a wider role for this cortical area than just gustatory coding.(ABSTRACT TRUNCATED AT 400 WORDS)


1997 ◽  
Vol 78 (4) ◽  
pp. 1913-1927 ◽  
Author(s):  
Sergio Masetto ◽  
Manning J. Correia

Masetto, Sergio and Manning J. Correia. Electrophysiological properties of vestibular sensory and supporting cells in the labyrinth slice before and during regeneration. J. Neurophysiol. 78: 1913–1927, 1997. The whole cell patch-clamp technique in combination with the slice preparation was used to investigate the electrophysiological properties of pigeon semicircular canal sensory and supporting cells. These properties were also characterized in regenerating neuroepithelia of pigeons preinjected with streptomycin to kill the hair cells. Type II hair cells from each of the three semicircular canals showed similar, topographically related patterns of passive and active membrane properties. Hair cells located in the peripheral regions (zone I, near the planum semilunatum) had less negative resting potentials [0-current voltage in current-clamp mode ( V z) = −62.8 ± 8.7 mV, mean ± SD; n = 13] and smaller membrane capacitances ( C m = 5.0 ± 0.9 pF, n = 14) than cells of the intermediate (zone II; V z = −79.3 ± 7.5 mV, n = 3; C m = 5.9 ± 1.2 pF, n = 4) and central (zone III; V z = −68.0 ± 9.6 mV, n = 17; C m = 7.1 ± 1.5 pF, n = 18) regions. In peripheral hair cells, ionic currents were dominated by a rapidly activating/inactivating outward K+ current, presumably an A-type K+ current ( I KA). Little or no inwardly rectifying current was present in these cells. Conversely, ionic currents of central hair cells were dominated by a slowly activating/inactivating outward K+ current resembling a delayed rectifier K+ current ( I KD). Moreover, an inward rectifying current at voltages negative to −80 mV was present in all central cells. This current was composed of two components: a slowly activating, noninactivating component ( I h), described in photoreceptors and saccular hair cells, and a faster-activating, partially inactivating component ( I K1) also described in saccular hair cells in some species. I h and I K1 were sometimes independently expressed by hair cells. Hair cells located in the intermediate region (zone II) had ionic currents more similar to those of central hair cells than peripheral hair cells. Outward currents in intermediate hair cells activated only slightly more quickly than those of the cells of the central region, but much more slowly than those of the peripheral cells. Additionally, intermediate hair cells, like central hair cells, always expressed an inward rectifying current. The regional distribution of outward rectifying potassium conductances resulted in macroscopic currents differing in peak–to–steady state ratio. We quantified this by measuring the peak ( G p) and steady-state ( G s) slope conductance in the linear region of the current-voltage relationship (−40 to 0 mV) for the hair cells located in the different zones. G p/ G s average values (4.1 ± 2.1, n = 15) from currents in peripheral hair cells were higher than those from intermediate hair cells (2.3 ± 0.8, n = 4) and central hair cells(1.9 ± 0.8, n = 21). The statistically significant differences ( P < 0.001) in G p/ G s ratios could be accounted for by KA channels being preferentially expressed in peripheral hair cells. Hair cell electrophysiological properties in animals pretreated with streptomycin were investigated at ∼3 wk and ∼9–10 wk post injection sequence (PIS). At 3 wk PIS, hair cells (all zones combined) had a statistically significantly ( P < 0.001) lower C m (4.6 ± 1.1 pF, n = 24) and a statistically significantly ( P < 0.01) lower G p(48.4 ± 20.8 nS, n = 26) than control animals ( C m = 6.2 ± 1.6 pF, n = 36; G p = 66 ± 38.9 nS, n = 40). Regional differences in values of V z, as well as the distribution of outward and inward rectifying currents, seen in control animals, were still obvious. But, differences in the relative contribution of the expression of the different ionic current components changed. This result could be explained by a relative decrease in I KA compared with I KD during that interval of regeneration, which was particularly evident in peripheral hair cells. At 9–10 wk PIS, hair cells of all zones had membrane properties not statistically different ( P > 0.5) from those in untreated normal animals. C m was 6.1 ± 1.3 pF ( n = 30) and G p was 75.9 ± 36.6 nS ( n = 30). Thus it appears that during regeneration, avian semicircular canal type II hair cells are likely to recover all their functional properties. At 9–10 wk PIS, regenerated hair cells expressed the same macroscopic ionic currents and had the same topographic distribution as normal hair cells. Measurements obtained at 3 wk PIS suggest that regenerated hair cells come from smaller cells (smaller mean values of C m) endowed with fewer potassium channels (smaller mean values of G p). In addition, differences observed in peripheral hair cells' kinetics and G p/ G s ratios at 3 wk PIS suggest that different ionic channels follow different schedules of expression during hair cell regeneration. We recorded from nine supporting cells both in normal ( n = 5) and regenerating ( n = 4) epithelia. These cells had an average negative resting potential of V z = −49.5 ± 14.1 mV ( n = 9), but no obvious sign of voltage- and time-dependent ionic currents, except for a very weak inward rectification at very negative potentials, both in normal and streptomycin-recovering animals. Therefore, if all semicircular canal supporting cells are like the small sample we tested and if supporting cells are actually the progenitors of regenerating hair cells, then they must change shape, develop hair bundles, become reinnervated, and also acquire a complete set of ionic channels ex novo.


2008 ◽  
Vol 99 (3) ◽  
pp. 1366-1379 ◽  
Author(s):  
Yuzhi Chen ◽  
Wilson S. Geisler ◽  
Eyal Seidemann

Behavioral performance in detection and discrimination tasks is likely to be limited by the quality and nature of the signals carried by populations of neurons in early sensory cortical areas. Here we used voltage-sensitive dye imaging (VSDI) to directly measure neural population responses in the primary visual cortex (V1) of monkeys performing a reaction-time detection task. Focusing on the temporal properties of the population responses, we found that V1 responses are consistent with a stimulus-evoked response with amplitude and latency that depend on target contrast and a stimulus-independent additive noise with long-lasting temporal correlations. The noise had much lower amplitude than the ongoing activity reported previously in anesthetized animals. To understand the implications of these properties for subsequent processing stages that mediate behavior, we derived the Bayesian ideal observer that specifies how to optimally use neural responses in reaction time tasks. Using the ideal observer analysis, we show that 1) the observed temporal correlations limit the performance benefit that can be attained by accumulating V1 responses over time, 2) a simple temporal decorrelation operation with time-lagged excitation and inhibition minimizes the detrimental effect of these correlations, 3) the neural information relevant for target detection is concentrated in the initial response following stimulus onset, and 4) a decoder that optimally uses V1 responses far outperforms the monkey in both speed and accuracy. Finally, we demonstrate that for our particular detection task, temporal decorrelation followed by an appropriate running integrator can approach the speed and accuracy of the optimal decoder.


1985 ◽  
Vol 53 (6) ◽  
pp. 1356-1369 ◽  
Author(s):  
T. Yamamoto ◽  
N. Yuyama ◽  
T. Kato ◽  
Y. Kawamura

The present report was designed to investigate neural coding of taste information in the cerebral cortical taste area of rats. The magnitude and/or type (excitatory, inhibitory, or no-response) of responses of 111 cortical neurons evoked by single concentrations of the four basic taste stimuli (sucrose, NaCl, HCl, and quinine HCl) were subjected to four types of analyses in the context of the four proposed hypotheses of taste-quality coding: across-neuron response-pattern, labeled-line, matrix-pattern, and across-region response-pattern notions (88 histologically located neurons). An across-neuron response-pattern notion assumes that taste quality is coded by differential magnitudes of response across many neurons. This theory utilizes across-neuron correlation coefficients as a metric for the evaluation of taste quality coding. Across-neuron correlations between magnitudes of responses to any pairs of the four basic taste stimuli across 111 cortical neurons were very high and were similar. However, calculations made with net responses (spontaneous rate subtracted) resulted in less positive correlations but still similar values among the various pairs of taste stimuli. This finding suggests that across-neuron response patterns of cortical neurons become less discriminating among taste qualities compared with those of the lower-order neurons. A labeled-line notion assumes that there are identifiable groups of neurons and that taste quality is coded by activity in these particular sets of neurons. Some investigators have classified taste-responsive neurons into best-stimulus categories, depending on their best sensitivity to any one of the four basic stimuli, such as sucrose-best, NaCl-best, HCl-best, and quinine-best neurons; they have suggested that taste can be classified along four qualitative dimensions that correspond to these four neuron types (i.e., four labeled lines). The present study shows that responsiveness of each of the four best-stimulus neurons had similar profiles between peripheral and cortical levels. That is, when the stimuli were arranged along the abscissa in the order of sucrose, NaCl, HCl, and quinine, there is a peak response in one place, and the responses decreased gradually from the peak. However, such response characteristics do not favor the labeled-line theory, since they can be explained in the context of the across-neuron pattern theory. A matrix-pattern notion assumes that taste quality is coded by a spatially arranged matrix pattern of activated neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


2000 ◽  
Vol 84 (4) ◽  
pp. 2048-2062 ◽  
Author(s):  
Mitesh K. Kapadia ◽  
Gerald Westheimer ◽  
Charles D. Gilbert

To examine the role of primary visual cortex in visuospatial integration, we studied the spatial arrangement of contextual interactions in the response properties of neurons in primary visual cortex of alert monkeys and in human perception. We found a spatial segregation of opposing contextual interactions. At the level of cortical neurons, excitatory interactions were located along the ends of receptive fields, while inhibitory interactions were strongest along the orthogonal axis. Parallel psychophysical studies in human observers showed opposing contextual interactions surrounding a target line with a similar spatial distribution. The results suggest that V1 neurons can participate in multiple perceptual processes via spatially segregated and functionally distinct components of their receptive fields.


2013 ◽  
Vol 110 (5) ◽  
pp. 1190-1204 ◽  
Author(s):  
Maria Ter-Mikaelian ◽  
Malcolm N. Semple ◽  
Dan H. Sanes

Animal communication sounds contain spectrotemporal fluctuations that provide powerful cues for detection and discrimination. Human perception of speech is influenced both by spectral and temporal acoustic features but is most critically dependent on envelope information. To investigate the neural coding principles underlying the perception of communication sounds, we explored the effect of disrupting the spectral or temporal content of five different gerbil call types on neural responses in the awake gerbil's primary auditory cortex (AI). The vocalizations were impoverished spectrally by reduction to 4 or 16 channels of band-passed noise. For this acoustic manipulation, an average firing rate of the neuron did not carry sufficient information to distinguish between call types. In contrast, the discharge patterns of individual AI neurons reliably categorized vocalizations composed of only four spectral bands with the appropriate natural token. The pooled responses of small populations of AI cells classified spectrally disrupted and natural calls with an accuracy that paralleled human performance on an analogous speech task. To assess whether discharge pattern was robust to temporal perturbations of an individual call, vocalizations were disrupted by time-reversing segments of variable duration. For this acoustic manipulation, cortical neurons were relatively insensitive to short reversal lengths. Consistent with human perception of speech, these results indicate that the stable representation of communication sounds in AI is more dependent on sensitivity to slow temporal envelopes than on spectral detail.


1994 ◽  
Vol 72 (6) ◽  
pp. 2827-2839 ◽  
Author(s):  
P. J. Istvan ◽  
P. Zarzecki

1. Discharge patterns of neurons are regulated by synaptic inputs and by intrinsic membrane properties such as their complement of ionic conductances. Discharge patterns evoked by synaptic inputs are often used to identify the source and modality of sensory input. However, the interpretation of these discharge patterns may be complicated if different neurons respond to the same synaptic input with a variety of discharge patterns due to differences in intrinsic membrane properties. The purposes of this study were 1) to investigate intrinsic discharge patterns of neurons in primary somatosensory cortex of raccoon in vivo and 2) to use somatosensory postsynaptic potentials evoked by stimulation of forepaw digits to determine thalamocortical connectivity for the same neurons. 2. Conventional intracellular recordings with sharp electrodes were made from 121 neurons in the cortical representation of glabrous skin of digit four (d4). Intracellular injection of identical current pulses (100-120 ms in duration) elicited various patterns of discharge in different neurons. Neurons were classified on the basis of these intrinsic patterns of discharge, rates of spike adaptation, and characteristics of spike waveforms. Three main groups were identified: regular spiking (RS) neurons, intrinsic bursting (IB) neurons, and fast spiking (FS) neurons. Subclasses were identified for the RS and IB groups. 3. Neurons were tested for somatosensory inputs by stimulating electrically d3, d4, and d5. Excitatory postsynaptic potentials (EPSPs) were elicited in 100% of the neurons by electrical stimulation of d4, the "on-focus" digit. EPSPs were usually followed by inhibitory postsynaptic potentials (IPSPs). Many neurons (41%) responded with EPSP-IPSP sequences after stimulation of d3 or d5, the "off-focus" digits. 4. Latencies of somatosensory EPSPs and IPSPs were used to determine the synaptic order in the cortical circuitry of RS, IB, and FS neurons. EPSPs with monosynaptic thalamocortical latencies were recorded in RS, IB, and FS neurons. 5. We conclude that precise patterns of neural discharge in primary somatosensory cortex cannot be reliable estimates of sensory inputs reaching these neurons because patterns of discharge are so strongly influenced by intrinsic membrane properties. Ionic conductances governing patterns of neuronal discharge seem almost identical in intact cortex of raccoon, rat, and cat, and in slices of rodent cortex, because similar patterns of discharge are found. The consistency of patterns of discharge across species and types of preparation suggests that these intrinsic membrane properties are a general property of cerebral cortical neurons and should be considered when evaluation sensory coding by these neurons.


2015 ◽  
Vol 27 (2) ◽  
pp. 255-280 ◽  
Author(s):  
Yang Qi ◽  
Michael Breakspear ◽  
Pulin Gong

Bump attractors are localized activity patterns that can self-sustain after stimulus presentation, and they are regarded as the neural substrate for a host of perceptual and cognitive processes. One of the characteristic features of bump attractors is that they are neutrally stable, so that noisy inputs cause them to drift away from their initial locations, severely impairing the accuracy of bump location-dependent neural coding. Previous modeling studies of such noise-induced drifting activity of bump attractors have focused on normal diffusive dynamics, often with an assumption that noisy inputs are uncorrelated. Here we show that long-range temporal correlations and spatial correlations in neural inputs generated by multiple interacting bumps cause them to drift in an anomalous subdiffusive way. This mechanism for generating subdiffusive dynamics of bump attractors is further analyzed based on a generalized Langevin equation. We demonstrate that subdiffusive dynamics can significantly improve the coding accuracy of bump attractors, since the variance of the bump displacement increases sublinearly over time and is much smaller than that of normal diffusion. Furthermore, we reanalyze existing psychophysical data concerning the spread of recalled cue position in spatial working memory tasks and show that its variance increases sublinearly with time, consistent with subdiffusive dynamics of bump attractors. Based on the probability density function of bump position, we also show that the subdiffusive dynamics result in a long-tailed decay of firing rate, greatly extending the duration of persistent activity.


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