Functional Role of Corticogeniculate Feedback in Vision
In mammals, all conscious visual information traverses a path from the retina through the visual thalamus (called the lateral geniculate nucleus or LGN) to the primary visual cortex (V1). Accordingly, in just a handful of synapses and in about 50 milliseconds, information about a visual stimulus in the world can reach the cortex. In highly visual mammals such as humans, visual information traversing this path is segregated into three parallel processing streams. By separating out visual information that is most relevant for processing motion, form/acuity, and color, signals can be relayed in parallel for increased processing speed. Even though parallel stream segregation is a hallmark of the early visual pathways in highly visual mammals, we are not aware of this separation of visual information because signals from the parallel streams are combined in the visual cortex. We tend to think about visual information encoding as a feedforward process in which information progresses from lower visual areas, such as the LGN and V1, to visual cortical areas higher up in the processing hierarchy. However, the circuits of the visual system include many feedback projections in addition to the more commonly studied feedforward projections.
The first feedback circuit in the visual system is the corticogeniculate circuit connecting V1 to the LGN in the feedback direction. Corticogeniculate circuits are actually a subset of the larger family of corticothalamic circuits that link primary sensory cortex with the sensory thalamus in the feedback direction. As such, corticogeniculate circuits, and corticothalamic circuits in general, are thought to play an important role in regulating the feedforward flow of sensory information. In spite of many decades of study, the functional role of corticothalamic feedback in sensory perception has remained a fundamental mystery in systems neuroscience. Part of the difficulty in defining the functional role of corticothalamic feedback is due to the fact that these feedback circuits appear to merely modulate, rather than drive, changes in thalamic responses. In the visual system, corticogeniculate inputs onto LGN relay neurons far outnumber retinal inputs onto LGN relay neurons. However, LGN relay neurons have receptive field properties that mimic their retinal and not their cortical inputs. Are LGN relay neurons simply “relaying” (as their name would imply) retinal signals to the cortex, or is there some purpose for having a layover in the thalamus, midway between the retina and the cortex?
We have been dedicated to cracking the mystery of corticogeniculate feedback for many years. We previously discovered that corticogeniculate feedback is made up of multiple morphologically and physiologically distinct cell types (see Briggs et al., 2016; Briggs & Usrey, 2005, 2007, 2009). Interestingly, these distinct cell types map precisely onto the distinct feedforward streams that are the hallmark of the early visual pathways. We hypothesized that corticogeniculate feedback is carrying stream-specific information from V1 back to the LGN. But to what purpose?
Recently, we utilized an innovative combination of virus-mediated gene delivery and optogenetics to selectively and reversibly control the activity of corticogeniculate neurons in vivo. We discovered that enhancing corticogeniculate feedback dramatically reduced the response latency of LGN relay neurons to incoming visual inputs (Hasse & Briggs, 2017). In addition to responding more quickly to visual inputs, LGN neurons also responded more precisely and their receptive fields narrowed. Interestingly, we did not observe any changes in the tuning properties of LGN neurons with enhanced corticogeniculate feedback. Our results therefore confirm that corticogeniculate feedback is not responsible for driving the response properties of LGN neurons. Instead, corticogeniculate feedback controls the timing and precision of LGN responses to incoming visual information. We believe these findings will generalize to corticothalamic circuits across sensory modalities and perhaps extend to feedback circuits throughout the brain. Future research is aimed at understanding whether and how corticogeniculate feedback controls the timing of LGN responses in a stream-specific manner.
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