Lack of robust LGN label following transneuronal rabies virus injections into macaque area V4

Abstract

In primates, retinal inputs are relayed through the magno- and parvocells of the lateral geniculate nucleus (LGN) indirectly to extrastriate visual cortex. The most direct pathway identified to the extrastriate cortex is a disynaptic one that provides robust magno- and parvocellular inputs to the middle temporal area (MT). The inclusion of parvocells in this projection is somewhat surprising because of their importance for color and form vision, whereas MT is more strictly tuned to velocity. This raises the question of whether areas more involved in color and form processing, such as V4, receive similar projections. We report here on experiments that use rabies virus injections into V4 to retrogradely label mono- and disynaptic inputs. We find only a small number of labeled neurons in the LGN in a pattern consistent with monosynaptic labeling of koniocells, rather than disynaptic labeling of magno- and parvocells. The lack of robust magno- and parvocellular label was not due to ineffective viral transport because in the same cases we find hundreds of neurons labeled in the thalamic reticular nucleus, a structure that can only be labeled disynaptically from the cortex. We also find a complete absence of neurons labeled in V1, but thousands in adjacent areas V2 and V3. This result helps explain the absence of labeled magno- and parvocells in the LGN because disynaptic transport from an extrastriate visual area should require a relay through V1. Taken together, these results suggest that ascending magno/parvocellular inputs to V4 are more hierarchically organized than the relatively direct inputs to MT.

Thalamic projections to visual and visuomotor areas (V6 and V6A) in the Rostral Bank of the parieto-occipital sulcus of the Macaque

“…The primary visual area was classically considered the main target of LGN in primates (Hubel and Wiesel 1972), though there is currently considerable evidence of sparse connections from the LGN to extrastriate areas (Wong-Riley 1976;Benevento and Yoshida 1981;Yukie and Iwai 1981;Bullier and Kennedy 1983;Lysakowski et al 1988;Hernandez-Gonzalez et al 1994;Sincich et al 2004;Warner et al 2010;Lyon and Rabideau 2012). Present results are in line with this evidence, which may be important to explain the residual visual function that remains in cases of cortical blindness after striate cortex lesions (Schmid et al 2010;Yu et al 2013).…”

Very-long-range disynaptic V1 connections through layer 6 pyramidal neurons revealed by transneuronal tracing with rabies virus

“…The titer of our virus (~1×10 7 PFU/mL) was lower than that of the CVS-11 virus used by Kelly and Strick,52 who confirmed that a 72-hour survival time limited infection to second-order neurons. Similar controls for our lower-titer virus were used in three previous publications 49,53,54. Therefore, it is highly unlikely that our lower-titer virus would have infected beyond two synapses.…”

V1 connections reveal a series of elongated higher visual areas in the California ground squirrel, Otospermophilus beecheyi

“…Therefore, labeled cell bodies are readily identifiable, which for large brain sections such as flattened squirrel cortex can be easier to detect compared to smaller terminals labeled by anterograde tracers. Furthermore, rabies virus infects specifically through synaptic terminals (Lafon, 2005) and therefore does not get taken up by axons of passage unlike standard retrograde and anterograde tracers (Callaway, 2008;Kelly & Strick, 2000;Lyon, Nassi, & Callaway, 2010;Lyon & Rabideau, 2012;Nassi, Lyon, & Callaway, 2006;Ugolini, 1995). Furthermore, rabies virus infects specifically through synaptic terminals (Lafon, 2005) and therefore does not get taken up by axons of passage unlike standard retrograde and anterograde tracers (Callaway, 2008;Kelly & Strick, 2000;Lyon, Nassi, & Callaway, 2010;Lyon & Rabideau, 2012;Nassi, Lyon, & Callaway, 2006;Ugolini, 1995).…”