title: A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex.
abstract: How specific features in the environment are represented within the brain is an important unanswered question in neuroscience. A subset of retinal neurons, called direction-selective ganglion cells (DSGCs), are specialized for detecting motion along specific axes of the visual field. Despite extensive study of the retinal circuitry that endows DSGCs with their unique tuning properties, their downstream circuitry in the brain and thus their contribution to visual processing has remained unclear. In mice, several different types of DSGCs connect to the dorsal lateral geniculate nucleus (dLGN), the visual thalamic structure that harbours cortical relay neurons. Whether direction-selective information computed at the level of the retina is routed to cortical circuits and integrated with other visual channels, however, is unknown. Here we show that there is a di-synaptic circuit linking DSGCs with the superficial layers of the primary visual cortex (V1) by using viral trans-synaptic circuit mapping and functional imaging of visually driven calcium signals in thalamocortical axons. This circuit pools information from several types of DSGCs, converges in a specialized subdivision of the dLGN, and delivers direction-tuned and orientation-tuned signals to superficial V1. Notably, this circuit is anatomically segregated from the retino-geniculo-cortical pathway carrying non-direction-tuned visual information to deeper layers of V1, such as layer 4. Thus, the mouse harbours several functionally specialized, parallel retino-geniculo-cortical pathways, one of which originates with retinal DSGCs and delivers direction- and orientation-tuned information specifically to the superficial layers of the primary visual cortex. These data provide evidence that direction and orientation selectivity of some V1 neurons may be influenced by the activation of DSGCs.
authors.affiliation: 1] Department of Neurosciences, University of California, San Diego, California 92093, USA [2] Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA.
authors.forename: Alberto
authors.initials: A
authors.lastname: Cruz-Martín
authors.affiliation: 1] Department of Neurosciences, University of California, San Diego, California 92093, USA [2] Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA.
authors.forename: Rana N
authors.initials: RN
authors.lastname: El-Danaf
authors.affiliation: Salk Institute for Biological Studies, La Jolla, California 92097, USA.
authors.forename: Fumitaka
authors.initials: F
authors.lastname: Osakada
authors.affiliation: Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA.
authors.forename: Balaji
authors.initials: B
authors.lastname: Sriram
authors.affiliation: 1] Department of Neurosciences, University of California, San Diego, California 92093, USA [2] Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA.
authors.forename: Onkar S
authors.initials: OS
authors.lastname: Dhande
authors.affiliation: 1] Department of Neurosciences, University of California, San Diego, California 92093, USA [2] Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA.
authors.forename: Phong L
authors.initials: PL
authors.lastname: Nguyen
authors.affiliation: Salk Institute for Biological Studies, La Jolla, California 92097, USA.
authors.forename: Edward M
authors.initials: EM
authors.lastname: Callaway
authors.affiliation: Neuroscience Discovery, F. Hoffman La Roche, 4070 Basel, Switzerland.
authors.forename: Anirvan
authors.initials: A
authors.lastname: Ghosh
authors.affiliation: 1] Department of Neurosciences, University of California, San Diego, California 92093, USA [2] Neurobiology Section in the Division of Biological Sciences, University of California, San Diego, California 92093, USA [3] Salk Institute for Biological Studies, La Jolla, California 92097, USA [4] Department of Ophthalmology, University of California, San Diego, California 92093, USA.
authors.forename: Andrew D
authors.initials: AD
authors.lastname: Huberman
mesh_terms: D000818:Animals; D001369:Axons / Q000502:physiology; D020013:Calcium Signaling; D005829:Geniculate Bodies / Q000166:cytology / Q000502:physiology; D057809:HEK293 Cells; D006801:Humans; D051379:Mice; D009434:Neural Pathways / Q000502:physiology*; D009949:Orientation / Q000502:physiology; D011820:Rabies virus / Q000235:genetics / Q000502:physiology; D012165:Retinal Ganglion Cells / Q000166:cytology* / Q000502:physiology*; D013788:Thalamus / Q000166:cytology / Q000502:physiology; D014793:Visual Cortex / Q000166:cytology* / Q000502:physiology*