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Comparative Study
, 26 (16), 4444-50

Attentional Modulation of Thalamic Reticular Neurons

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Comparative Study

Attentional Modulation of Thalamic Reticular Neurons

Kerry McAlonan et al. J Neurosci.

Abstract

The major pathway for visual information reaching cerebral cortex is through the lateral geniculate nucleus (LGN) of the thalamus. Acting on this vital relay is another thalamic nucleus, the thalamic reticular nucleus (TRN). This nucleus receives topographically organized collaterals from both thalamus and cortex and sends similarly organized projections back to thalamus. The inputs to the TRN are excitatory, but the output back to the thalamic relay is inhibitory, providing an ideal organization for modulating visual activity during early processing. This functional architecture led Crick in 1984 to hypothesize that TRN serves to direct a searchlight of attention to different regions of the topographic map; however, despite the substantial influence of this hypothesis, the activity of TRN neurons has never been determined during an attention task. We have determined the nature of the response of visual TRN neurons in awake monkeys, and the modulation of that response as the monkeys shifted attention between visual and auditory stimuli. Visual TRN neurons had a strong (194 spikes/s) and fast (25 ms latency) transient increase of activity to spots of light falling in their receptive fields, as well as high background firing rate (45 spikes/s). When attention shifted to the spots of light, the amplitude of the transient visual response typically increased, whereas other neuronal response characteristics remained unchanged. Thus, as predicted previously, TRN activity is modified by shifts of visual attention, and these attentional changes could influence visual processing in LGN via the inhibitory connections back to the thalamus.

Figures

Figure 1.
Figure 1.
Cross-modal attention task. The color of the fixation point indicated whether a given trial was a visual trial or an auditory trial. A green fixation point meant a visual trial, and the monkey was to attend to the visual stimulus (a spot in the receptive field of the TRN neuron). A red fixation point denoted an auditory trial, and the monkey was to attend to the auditory stimulus (a tone). During both visual and auditory trials, the visual spot either dimmed or remained constant, and, independently, the auditory tone either dimmed or remained constant. The possible dimming of either stimulus did not depend on the trial type. The monkey was rewarded by correctly reporting whether the attended stimulus (indicated by the color of the fixation point) dimmed or not. For details, see Materials and Methods.
Figure 2.
Figure 2.
Transient visual response of TRN neurons in the awake monkey. The superimposed transient visual responses of each of the 36 visual TRN neurons after the onset of a high-contrast spot of light centered in the receptive field of the neuron are aligned on stimulus onset at time 0. Each gray line is a spike density plot showing the mean of at least 27 stimulus presentations (mean number of presentations, 64). The thicker black line indicates the mean response for all 36 neurons. Note that each of the individual responses resembles a scaled version of the mean response, demonstrating the consistency of response latency and duration for TRN neurons.
Figure 3.
Figure 3.
Location of visual TRN neurons recorded in the awake monkey. Site of a visual TRN neuron marked by passing current through the recording microelectrode. Successive enlargements of the Nissl-stained coronal section show the location of the lesion. The pulvinar (PUL) and TRN have been labeled for reference.
Figure 4.
Figure 4.
Modulation of the visual response by attention. A, Visual responses of an example TRN neuron when the monkey was instructed to attend to the visual stimulus (top recording) and when it attended to the auditory stimulus (bottom recording). Only responses for correct trials are shown. For each trial type, spike density plots are superimposed on the spike rasters. The spike density plot for visual attention trials is duplicated in the bottom panel to facilitate comparison between the two cases. The arrow in each panel indicates the peak visual response (before subtracting background activity). The peak visual response was greater when the monkey attended to the visual stimulus. B, Difference in response when the visual stimulus is attended. The black trace is the difference between the spike density plots in the top and bottom panels of A (visual attended − auditory attended).
Figure 5.
Figure 5.
Change in visual response with attention in the sample of 36 neurons. A, Summary of differences in response for all 36 TRN neurons. The thick trace shows the mean change in response when the monkey shifted attention to the visual stimulus. Thin lines represent ± 1 SD of the differences. B, Distribution of response differences expressed as the proportion change in response between auditory and visual trials. The mean proportional increase in peak response (0.10, p = 0.007) is indicated by the arrow. C, Change in peak neuronal response for each TRN neuron. For each neuron, this plot shows the peak neuronal response during visual trials (when the monkey was instructed to attend to the visual stimulus) versus the peak neuronal response during auditory trials. Background activity was subtracted from all peak responses. Note that the abscissa and ordinate are both in log coordinates, so as not to overemphasize response differences at higher firing rates. Symbols with the top triangle filled indicate significant differences in peak visual response. Symbols with the bottom triangle filled denote experiments in which the monkey met the attentional psychophysical criteria.

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