The Connection from Cortical Area V1 to V5: A Light and Electron Microscopic Study

Abstract

Area V5 (middle temporal) in the superior temporal sulcus of macaque receives a direct projection from the primary visual cortex (V1). By injecting anterograde tracers (biotinylated dextran and Phaseolus vulgaris lectin) into V1, we have examined the synaptic boutons that they form in V5 in the electron microscope. Nearly 80% of the target cells in V5 were spiny (excitatory). The boutons formed asymmetric (Gray's type 1) synapses with spines (54%), dendrites (33%), and somata (13%). All somatic targets and some (26%) of the target dendritic shafts showed features characteristic of smooth (inhibitory) cells. Each bouton formed, on average, 1.7 synapses. The larger boutons formed multiple synapses with the same neuron and completely enveloped the entire spine head. On most dendritic shafts and all somata the postsynaptic density en face was disk-shaped but in about half the cases the reconstructed postsynaptic densities of synapses on spines appeared as complete or partial annuli. Even in the zones of densest innervation only 3% of the asymmetric synapses were formed by the labeled boutons. Although the V1 projection forms only a small minority of synapses in V5, its affect could be considerably amplified by local circuits in V5, in a way analogous to the amplification of the small thalamic input to area V1. Key words: visual cortex; area MT; corticocortical; synapse morphology; postsynaptic target; 3-D reconstructionThe best-studied extrastriate area is that first discovered by Zeki (1969), who used anatomical methods to define an area in the posterior bank of the superior temporal sulcus in macaque monkey that received an input from area 17. The homologous area in the new-world monkey is the middle temporal area (MT) (Allman and Kaas, 1971). From the earliest recordings, it was evident that the neurons of this area, now called MT or V5, were particularly sensitive to the direction and velocity of motion of the stimulus (Dubner and Z eki, 1971).There are both direct and indirect projections from V1 to area V5 (Z eki, 1969;Ungerleider and Mishkin, 1979;Maunsell and Van Essen, 1983;Fries et al., 1985). The neurons that project directly from V1 have been identified as spiny stellates and pyramidal cells in layer 4B and large pyramidal cells in upper layer 6 (L und et al., 1975;Shipp and Z eki, 1989). Their afferent axons form large boutons in a patchy distribution in layers 3, 4, and 6 of V5 (Rockland, 1989(Rockland, , 1995. The receptive fields of the V1 neurons that project to V5 have also been studied. The projecting neurons were identified by antidromically activating them from V5 (Movshon and Newsome, 1996). They had fastconducting axons and all were binocular, complex cells, with high-contrast sensitivity and contrast-independent direction preferences. They responded at least as well to short stimuli as to long stimuli. Such complex cells are referred to as special (Palmer and Rosenquist, 1974) and have the largest receptive fields, the highest velocity preference, and the highest spontaneity of striate corti...

The Synaptic Connections between Cortical Areas V1 and V2 in Macaque Monkey

“…Boutons are usually recognized as beads along an axon (bouton en passant) or swellings on short processes extending from the axon (bouton terminaux). Using correlated LM and EM we have repeatedly verified here, and in previous studies (Anderson et al, 1998;Anderson and Martin, 2002, 2005, 2006 that boutons identified at light microscope level form synaptic specializations and that synapses in the interbouton segments are rare.…”

“…Collections of serial sections were digitized and reconstructed using Trakem, an in-house EM-digitization package. To measure and display the postsynaptic densities of labeled boutons we used software developed by ourselves, which has been described in outline previously [see Anderson et al (1998), their Materials and Methods]. We used a Philips CM100 electron microscope fitted with a Morada camera and ITM software.…”

The role of long-range connections on the specificity of the macaque interareal cortical network

“…As shown here, these long-distance connections are important in characterizing the connectivity of regions and the individuality of the connectivity profiles of areas. It remains to be seen whether long-distance connections exhibit unique properties, such as synaptic morphologies (40) or molecular identities of the parent neurons (27,41,42). Overall, the present results point to the need to fully embrace the large-scale connectivity of the cortex if we are to resolve how its overall structural complexity relates to its function.…”

The Early Maturation of Visual Cortical Area MT is Dependent on Input from the Retinorecipient Medial Portion of the Inferior Pulvinar

“…Based on NNF labeling in the newborn marmoset, which is an indicator of pyramidal cell maturation, existing projections from V1 to area MT at birth are immature (Bourne et al, 2005). In addition, PV labeling, a marker for onset of neuronal activity (Hendrickson et al, 1991), is not present until between P7-P14 in layer 3C of V1 and layer 4 of MT (the V1 recipient layer) (Rockland 1989(Rockland , 1995Anderson et al, 1998). It is not until P90, the start of the "critical period" in the marmoset (Missler .…”

“…We specifically examined layer 3C of V1 as well as the input layers 3 and 4 of area MT with which both PIm and V1 terminate. The pulvinorecipient layer in area MT is primarily in deep layer 3 (Spatz, 1975;Trojanowski and Jacobson, 1976;Rockland 1989Rockland , 1995Anderson et al, 1998;Rockland et al, 1999).…”