Exploring the pulvinar path to visual cortex

Abstract

The primary pathway for visual signals from the retina to cerebral cortex is through the lateral geniculate nucleus of the thalamus to primary visual cortex. A second visual pathway has been postulated to pass through the thalamic pulvinar nucleus and to project to multiple regions of visual cortex. We have explored this second visual pathway using a method that allows us to identify the inputs and outputs of pulvinar neurons. Specifically, we applied microstimulation in the superficial layers of superior colliculus (SC) to test for orthodromic activation of pulvinar neurons receiving input from SC. We also microstimulated the cortical motion area MT and tested for antidromic activation of pulvinar to identify neurons projecting to MT (and to determine the presence of orthodromic input back to pulvinar). In this initial report, we concentrate on two observations. First, we find that there are clusters of neurons in the pulvinar that receive input from SC along with neurons that project to MT or receive input from MT. Second, we find that neurons with input from SC have characteristics of the SC superficial layers: they respond to visual stimuli but do not discharge before saccadic eye movements. Neurons projecting to MT respond similarly to these SC-input neurons, while those receiving input from MT more frequently show directional selectivity as does MT. These findings indicate the visual nature of the signals conveyed in this pathway and shed light on the functional role of the thalamus in a possible second visual pathway.

Figure 1

Studying the second visual pathway by identifying connected neurons in the pulvinar. A sagittal view of the macaque brain shows the configuration of recording and stimulating electrodes used to identify pulvinar neurons with connections to superior colliculus (SC) or area MT. A recording microelectrode is lowered into the pulvinar nucleus (Pulv). Once a single neuron is isolated, microstimulation is used to determine whether the cell receives input or sends output to either SC or MT (see Methods).

Figure 2

Regions of the pulvinar with neurons receiving from SC and neurons projecting to MT. Schematic shows a coronal cross-section through the pulvinar at the level where single-unit recording was concentrated, just posterior to the LGN. The visual subdivisions, PI and PL, are of greatest interest for connected cells. PM = medial pulvinar; PL = lateral pulvinar, PI = inferior pulvinar, br = brachium of the superior colliculus, TRN = thalamic reticular nucleus.

Figure 3

Pulvinar neurons with input from SC have visual but not presaccadic activity. The activity of a single example neuron with input from SC during the memory-guided saccade task. A) Activity is aligned on the appearance of the stimulus. The pulvinar neuron gives a brisk visual response. B) Activity is aligned on the beginning of the eye movement. The neuron has no significant presaccadic build-up or burst activity. In each panel, the spike density function is smoothed with an 8ms Gaussian.

Figure 4

Pulvinar neurons with input from MT are more likely to be directionally selective than are pulvinar neurons with output to MT. The visual responses to eight different directions of motion are shown for A) an example pulvinar neuron receiving input from MT and B) an example pulvinar neuron sending output to MT. Activity is aligned on the appearance of the stimulus.