Thalamic pathways for active vision

Abstract

Active vision requires the integration of information coming from the retina with that generated internally within the brain, especially by saccadic eye movements. Just as visual information reaches cortex via the lateral geniculate nucleus of the thalamus, this internal information reaches the cerebral cortex through other higher-order nuclei of the thalamus. This review summarizes recent work on four of these thalamic nuclei. The first two pathways convey internal information about upcoming saccades (a corollary discharge) and probably contribute to the neuronal mechanisms that underlie stable visual perception. The second two pathways might contribute to the neuronal mechanisms underlying visual spatial attention in cortex and in the thalamus itself.

Figure 1

Pathways through the thalamus from the superior colliculus (SC) to cerebral cortex. Side view of a monkey brain highlighting thalamic nuclei that convey visual and/or saccade related activity in SC. A. A pathway that may carry a signal related to maintaining stable visual perception despite the image displacements produced by saccades. The pathway from saccade related neurons in the intermediate layers of superior colliculus (SC) passes through the lateral parvocellular region of the thalamic medial dorsal nucleus (MD) before reaching the frontal eye field (FEF) in frontal cortex. B. A pathway that may carry a signal that contributes to the suppression of blur during a saccade. The pathway originates in the visual neurons in the superficial layers, which project to inferior pulvinar (PI) and then to regions of occipital and parietal cortex, including the middle temporal area (MT). C. A pathway that may carry the preparatory movement related activity providing the motor signal for modulating visual cortical activity with shifts of visual attention. The candidate pathway is from the saccade related intermediate SC layers to the pulvinar (probably the lateral pulvinar (PL) and area Pdm at the border of lateral and medial pulvinar) and then to parietal and occipital cortex. D. The connections between the thalamic reticular nucleus (TRN) and the lateral geniculate nucleus (LGN), which may underlie the enhanced activity in the LGN with shifts of attention. The nature of the projections to both nuclei from the SC is uncertain. Thalamus representation after Netter [70]

Figure 2

The concept of a corollary discharge (CD) and its relation to thalamic function. A. The logic of a CD or efference copy (see main text). B. Applicability of CD to the SC and its pathways through thalamus to cerebral cortex. SC is part of the pathway descending to the lower midbrain and pons (downward arrow) and eventually to the motor neurons that move the eyes. A copy of this downward projection is directed upward to convey the movement information to other regions of the brain.

Figure 3

Use of a CD to anticipate the visual consequences of a saccade. A. Experimental design for demonstrating shifting RF activity. While the monkey is looking at the fixation spot, the RF activity is determined by flashing a spot, and the activity in the future field is also determined by such a spot. These responses are determined both long before the monkey makes a saccade to the target and just before the saccade onset. B. Example of shifting RF activity in FEF in black traces, and after MD inactivation in orange traces. Just before the saccade (right column) there was activity in the future field (right column upper row), but this was eliminated by inactivation of neurons in MD by injection of muscimol. This is consistent with the hypothesis that the information for the location of the future field is derived from a CD and that the CD used by FEF is derived from the SC-MD-FEF circuit. After Sommer and Wurtz [14].

Figure 4

Saccadic suppression in SC and PI. The top panel shows an example neuron from one of the original studies of suppression in the superficial SC. The eye trace at the top shows horizontal eye position; rasters and histograms below are aligned on saccade start (thin vertical line). Rasters show spikes in individual trials. The bottom panel shows an example neuron recorded from within the PI relay. The spike density function is aligned on saccade start. Horizontal lines indicate 100ms intervals. The SC and PI neurons each show a saccadic suppression of background activity. Reproduced with permission from Richmond and Wurtz [32] and Berman and Wurtz [28].

Figure 5

Modulation of visual attention in a change blindness task by stimulation of the SC neurons that are active before saccadic eye movements. A. Shift of attention by SC stimulation rather than by a visual cue. Stimulation began 300 msec before the blank period and continued for 600 ms, ending 150 ms after the motion patches reappeared. Stimulation current and pulse frequency were well below levels required to elicit saccades. In this example, the change in motion direction occurred in the upper left patch of dots (gray arrow). B. Sample results for an experiment showing stimulation overlapping a patch of moving dots (solid dots and upper drawing) and non-overlapping stimulation (open dots and lower drawing). Change in motion direction for this experiment was 40° and stimulation was always at the same SC location. When the target overlapped the site of SC stimulation, the proportion of hits increased, whereas when the target was non-overlapping, the hits did not change significantly (left plot). Reproduced with permission from Cavanaugh and Wurtz [52].

Figure 6

Modulation of visual activity in LGN and TRN by visual attention. A. Both the magnocellular (LGNm) and the parvocellular layers (LGNp) receive excitatory input from the retina and provide excitatory input to the TRN and V1. The TRN projection back to LGN is inhibitory. B. Increased visual response with attention into the RF of an LGNm and an LGNp neuron (increase of 12% and 24% respectively). C. Decreased TRN visual response with attention into the RF of the neuron (decrease of 13%). Horizontal lines in B, C indicate each neuron’s initial visual response. Attention changes the responses of both LGN and TRN neurons but in a reciprocal manner. Reproduced with permission from McAlonan, Cavanaugh and Wurtz [64].

Figure I, Box 1

Similarity of modulation of cortical activity by CD and by visual attention.