Abstract
Natural visual stimuli have highly structured spatial and temporal properties which influence the way visual information is encoded in the visual pathway. In response to natural scene stimuli, neurons in the lateral geniculate nucleus (LGN) are temporally precise – on a time scale of 10–25 ms – both within single cells and across cells within a population. This time scale, established by non stimulus-driven elements of neuronal firing, is significantly shorter than that of natural scenes, yet is critical for the neural representation of the spatial and temporal structure of the scene. Here, a generalized linear model (GLM) that combines stimulus-driven elements with spike-history dependence associated with intrinsic cellular dynamics is shown to predict the fine timing precision of LGN responses to natural scene stimuli, the corresponding correlation structure across nearby neurons in the population, and the continuous modulation of spike timing precision and latency across neurons. A single model captured the experimentally observed neural response, across different levels of contrasts and different classes of visual stimuli, through interactions between the stimulus correlation structure and the nonlinearity in spike generation and spike history dependence. Given the sensitivity of the thalamocortical synapse to closely timed spikes and the importance of fine timing precision for the faithful representation of natural scenes, the modulation of thalamic population timing over these time scales is likely important for cortical representations of the dynamic natural visual environment.
Highlights
Natural visual stimuli have highly structured spatial and temporal properties, which influence the way visual information is encoded in the visual pathway (Field, 1987; Atick and Redlich, 1992; van Hateren, 1992; Dong and Atick, 1995; Simoncelli and Olshausen, 2001)
As shown at the bottom of the panel, the variability in spiking activity that gives rise to the characteristic width of the peri-stimulus time histogram (PSTH) events can be decomposed into two distinct sources: (i) variability in the timing of a firing event from trial to trial and (ii) variability of spike times within each event, which we have described in detail previously (Desbordes et al, 2008), both of which having implications for the neural code
Previous modeling studies of early visual neurons have suggested that non stimulus-driven elements of neuronal firing are crucial in shaping the trial-averaged fine temporal precision of single cell response (Berry and Meister, 1998; Keat et al, 2001; Uzzell and Chichilnisky, 2004), which may be critical in faithfully encoding features of the more slowly varying natural scene (Butts et al, 2007)
Summary
Natural visual stimuli have highly structured spatial and temporal properties, which influence the way visual information is encoded in the visual pathway (Field, 1987; Atick and Redlich, 1992; van Hateren, 1992; Dong and Atick, 1995; Simoncelli and Olshausen, 2001). The timing of thalamic activity is significantly more precise than the time scale of the more slowly varying natural scene would dictate (Butts et al, 2007) This suggests that some elements of neuronal firing which are not stimulus-driven, such as the recent history of spiking (due to refractoriness, burstiness, fast adaptation, etc.), are crucial in shaping the fine temporal precision of early visual neurons (Berry and Meister, 1998; Keat et al, 2001). The fast time scale of the fine temporal precision of the neural response is necessary for the faithful representation of the more slowly varying natural scene (Butts et al, 2007), and is an important element of population models
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