Adaptation of Thalamic Neurons Provides Information about the Spatiotemporal Context of Stimulus History

Abstract

Adaptation of neural responses due to the history of sensory input has been observed across all sensory modalities. However, the computational role of adaptation is not fully understood, especially when one considers neural coding problems in which adaptation increases the ambiguity of the neural responses to simple stimuli. To address this, we quantified the impact of adaptation on the information conveyed by thalamic neurons about paired whisker stimuli in male rat. At the single neuron level, although paired-pulse adaptation reduces the information about the present stimulus, the information per spike increases. Moreover, the adapted response can convey significant amounts of information about whether, when and where a previous stimulus occurred. At the population level, ambiguity of the adapted responses about the present stimulus can be compensated for by large numbers of neurons. Therefore, paired-pulse adaptation does not reduce the discriminability of simple stimuli. It provides information about the spatiotemporal context of stimulus history.SIGNIFICANCE STATEMENT The present work provides a computational framework that demonstrates how adaptation allows neurons to encode spatiotemporal dynamics of stimulus history.

Keywords: encoding; in vivo; sensory coding; somatosensory; vibrissae; whiskers.

Figure 1.

Experimental procedure. Single-neuron responses were collected with two high-impedance tungsten electrodes E1 (gray) and E2 (black) lowered into the VPM nucleus of the thalamus. Paired stimuli were delivered to whisker stimulators W₁ (red) and W₂ (blue). The protocol included either same-whisker stimulation (i.e., repetitive in the same whisker with 50 or 100 ms interstimulus interval) or cross-whisker stimulation (i.e., cross from one whisker to the other with 50 or 100 ms interstimulus interval). Pairs of stimuli were separated with a 2 s interval for neurons to recovery from adaptation before proceeding to the next trial, with 200 trials per condition.

Figure 2.

Neurophysiological properties of VPM neurons to paired-pulse stimuli. A, Population responses of all 40 neurons; the top plots represent the population PSTH for the five groups of PW responses, whereas bottom plots represent the population PSTH for the five groups of SW responses. B, Response magnitude (RM) and (C) FF for the five groups of PW responses and the non-adapted SW response. The black stars indicate the significance levels for the post hoc Dunnett test for each adapted PW response and non-adapted SW response relative to the non-adapted PW response. *p < 0.05, **p < 0.01, ***p < 0.001. D, Scatter plot of FF versus RM. Inset, The average FF and RM of the VPM neurons in each group. E, The proportion of sub-Poisson, nearly Poisson, and supra-Poisson cells based on FF measurements in each group of PW responses. Error bars represent 95% confidence intervals.

Figure 3.

Information about stimulus location in the present carried by single neurons. A, Scatter plot of mutual information versus RM difference between PW stimulus (non-adapted or adapted) and SW stimulus. Inset, The average mutual information and RM difference for each group of adapted PW responses. B, Color map of percentage of autocorrelation information (% of total information), dependent on RM difference and FF difference between PW and SW stimulus. Error bars represent 95% confidence intervals.

Figure 4.

Information about stimulus history carried by single neurons. A, Mutual information for detecting whether a prior stimulus occurred, (B) Color map of percentage of autocorrelation information (% of total information) as a function of RM and FF differences between the adapted and non-adapted PW stimulus. The result is similar to Figure 3B. C, Mutual information to discriminate spatial context (_pwPW vs _swPW; red) and (D) temporal context (100 or 50 ms prior; blue) of the occurred previous stimulus. Error bars represent 95% confidence intervals. **p < 0.01.

Figure 5.

Information about stimulus location in the present carried by total number of spikes (solid line) or population response decoded with PSTH classification preserving neuron identities (dashed line). Information values are obtained from 100 permutations of random sampling of neurons. Boundary lines (light solid or light dashed) indicate 95% confidence intervals. A,B, Discriminating between adapted PW responses and SW response when the previous stimulus was the PW, 50 ms earlier (A) or 100 ms earlier (B). C, D, Discriminating between the adapted PW response and the SW response when the previous stimulus was SW, 50 ms earlier (C) or 100 ms earlier (D).

Figure 6.

Information rate (i.e., bits per spike) about stimulus location in the present carried by (A) total number of spikes or (B) population response decoded with PSTH classification preserving neuron identities.