The visual system of the brain of primates including humans includes two major pathways from the eye to the brain. One is from the retina through the lateral geniculate nucleus of the thalamus to primary visual area of the cerebral cortex A second path has been posited to provide an alternative route to cortex from the retina to the superficial layers of the superior colliculus (SC) in the brainstem,then on to a different thalamic nucleus, the pulvinar, and then to then to multiple visual areas of the cerebral cortex. The pulvinar is the largest nucleus that processes visual information in the thalamus, and it continues to be among the most perplexing. Much of what we know about the visual pulvinar comes from anatomical studies of its myriad subcortical and cortical connections, and these connections suggest an orderly organization, a clear functional parcellation has yet to emerge. We have recently identified a fucntional pathway through the pulvinar from superior colliculus to cortex, and have now concentrated on locating this pathway as it traverses the pulvinar and determining what signals it conveys. A major question centers on whether the pulvinar acts as a relay, particularly in the path from the superior colliculus (SC) to the motion area in middle temporal (MT) cortex. We used physiological microstimulation to identify pulvinar neurons belonging to the path from SC to MT in the macaque. We identified many neurons in the visual pulvinar that received input from SC or projected to MT, as well as a largely separate set of neurons that received input from MT. We then identified a subset of neurons as relay neurons that both received SC input and projected to MT. The identification of these relay neurons demonstrates a continuous functional path from SC to MT through the pulvinar in primates. Finally, we histologically localized a subset of SC-MT relay neurons to the subdivision of inferior pulvinar known to project densely to MT, but also localized SC-MT relay neurons to an adjacent subdivision. This pattern indicates that the pulvinar pathway is not limited to a single anatomically-defined region. We have now gone on to identify the signals conveyed by the pulvinar neurons to cortex. The general visual properties of the identified pulvinar neurons resembled those of SC visual neurons. They gave a burst of spikes at the onset of spots of light, showed indication of an inhibitory surround, and had relatively large receptive fields that increased with eccentricity. We observed little to no pre-saccadic activity. Two findings are salient. First, the pulvinar neurons convey only a subset of the visual modulations found in the SC: they exhibited saccadic suppression, the inhibition of activity at the time of the saccade, but did not show the attentional enhancement of the visual response seen in SC. Second, directional selectivity was minimal in pulvinar neurons belonging to the ascending path to MT but was significantly more prominent in pulvinar neurons receiving input from MT. This finding casts doubt on earlier assumptions that the pulvinar provides directionally-selective signals to MT and instead suggests that its selectivity is inherited from MT. The identification of this pathway and the signals it transmits establishes the first functional pathway from brainstem to cortex through pulvinar and makes it possible to examine the functional contribution of the pulvinar to cortical visual processing. Since the pulvinar is as prominent in the human brain as it is in the monkey brain, the pathway and signals conveyed in the monkey brain are highly like to be similar to that in the human brain. These experiments in the monkey therefore provide the first insights into the function of this large region of thalamus in the human brain

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Investigator-Initiated Intramural Research Projects (ZIA)
Project #
1ZIAEY000109-30
Application #
8149129
Study Section
Project Start
Project End
Budget Start
Budget End
Support Year
30
Fiscal Year
2010
Total Cost
$1,560,818
Indirect Cost
Name
U.S. National Eye Institute
Department
Type
DUNS #
City
State
Country
Zip Code
Cavanaugh, James; Berman, Rebecca A; Joiner, Wilsaan M et al. (2016) Saccadic Corollary Discharge Underlies Stable Visual Perception. J Neurosci 36:31-42
Wurtz, Robert H (2015) Using perturbations to identify the brain circuits underlying active vision. Philos Trans R Soc Lond B Biol Sci 370:
Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2013) Compression and suppression of shifting receptive field activity in frontal eye field neurons. J Neurosci 33:18259-69
Wurtz, Robert H (2013) Retrospective. David H. Hubel (1926-2013). Science 342:572
Joiner, Wilsaan Mychal; Cavanaugh, James; Fitzgibbon, Edmond J et al. (2013) Corollary Discharge Contributes To Perceived Eye Location In Monkeys. J Neurophysiol :
Cavanaugh, James; Monosov, Ilya E; McAlonan, Kerry et al. (2012) Optogenetic inactivation modifies monkey visuomotor behavior. Neuron 76:901-7
Cavanaugh, James; Joiner, Wilsaan M; Wurtz, Robert H (2012) Suppressive surrounds of receptive fields in monkey frontal eye field. J Neurosci 32:12284-93
Berman, Rebecca A; Wurtz, Robert H (2011) Signals conveyed in the pulvinar pathway from superior colliculus to cortical area MT. J Neurosci 31:373-84
Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2011) Modulation of shifting receptive field activity in frontal eye field by visual salience. J Neurophysiol 106:1179-90
Wurtz, Robert H; Joiner, Wilsaan M; Berman, Rebecca A (2011) Neuronal mechanisms for visual stability: progress and problems. Philos Trans R Soc Lond B Biol Sci 366:492-503

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