GABAergic projections from the pretectum boost retinogeniculate signal transfer via disinhibition.

Abstract

The transfer of retinal signals from the dorsal lateral geniculate nucleus (dLGN) to the primary visual cortex (V1) is modulated by a variety of extraretinal inputs, including extrinsic connections formed by GABAergic neurons in the pretectum (PT) and visual sector of the thalamic reticular nucleus (vTRN), as well as the intrinsic connections of GABAergic dLGN interneurons. In the current study, we determined how GABAergic PT projections to the dLGN and vTRN can influence retinogeniculate transfer using a variety of viral tracing techniques, electron microscopy, in vitro physiological recordings, and optogenetics in male and female mice. We found that the PT provides over 75% of the GABAergic, and over 30% of the total synaptic input to the vTRN. Optogenetic activation of PT terminals reduced the firing frequency of vTRN neurons as well as the amplitudes of their postsynaptic responses to V1 input. In the dLGN, synaptic terminals originating from the PT targeted interneurons more frequently than thalamocortical (relay) cells, and optogenetic activation of PT input had a greater impact on interneuron firing frequency compared to relay cells. This cell type specific impact of PT input to the dLGN resulted in the disinhibition of relay cells and an increase in the amplitude of their postsynaptic responses to retinal input. Taken together, our results indicate that GABAergic PT projections to the visual thalamus serve to boost retinogeniculate transfer via two types of disinhibition, potentially enhancing the flow of visual information to V1 following gaze shifts.Significance Statement The transfer of visual information from the retina to the cortex must be coordinated with gaze shifts to explore the surrounding environment. Here we document pathways from the pretectum, a region responsive during gaze shifts, to the visual thalamus. We find that pretectum neurons that use the inhibitory neurotransmitter gamma amino butyric acid (GABA) selectively innervate GABAergic neurons in the thalamic reticular nucleus and dorsal lateral geniculate nucleus, which serves to boost the transfer of visual information from the thalamus to the cortex. The identification of these brain circuits may have important implications for disorders of gaze shifts and/or sensory modulation.