Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido‐nigral complex in the monkey

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Abstract
To determine the organization of visual inputs and outputs of the striatum, we placed multiple retrograde and anterograde tracers into physiologically identified portions of the striatum known to receive inputs from visual cortex in seven macaques. The injection sites included the tail and genu of the caudate nucleus (14 cases), the head of the caudate (1 case), and the ventral putamen (3 cases). Retrogradely labeled cells were located predominantly in layer 5 of the ipsilateral cortex but were also found in layers 3 and 6. After caudate injections, labeled cells were found both in large, nearly continuous regions of cortex topographically related to the site of the injection, and in several smaller cortical regions that were discontinuous and common to many or all of the injection sites. The continuously labeled regions included nearly all known visual cortical areas, except for the striate cortex. After injections in the rostral tail, the continuously labeled region included the rostral portion of Bonin and Bailey's (Urbana: University of Illinois Press, 1947) area TE and adjacent portions of TF, TH, TG, and, occasionally, area 35 (Brodmann, Leipzig; J.A. Barth, '09). After injections into the posterior tail and ventral genu, the labeled region shifted posteriorly in TE and TF, and into TEO and the ventral parts of prestriate areas V4, V3, and (sparsely) V2. As the injection site was advanced into the dorsal genu, the labeled region shifted dorsally toward the parietal lobe, including prestriate areas MT and PO, parietal area PG (Brodmann's area 7), the ventral and lateral intraparietal sulcal areas (VIP and LIP, respectively), and area PE and adjacent area LC (Brodmann's areas 5 and 23, respectively). The discontinuous areas labeled by many different injections included the principal sulcus/frontal eye field region, the anterior cingulate cortex, and the superior temporal polysensory area. Thus, whereas temporal, occipital, and parietal visual cortical areas project into the caudate largely according to proximity, certain multimodal cortical areas seem to have a much wider projection. To determine whether visual cortical areas have additional projections to the caudate beyond the territory of our retrograde injection sites in the tail and genu, 3H-labeled amino acids were injected into areas TE, V4, and MT in three additional monkeys. The topographic location of label in the tail and genu of the caudate in these cases was consistent with the results from injections of retrograde tracers into the caudate. However, in addition to label in the tail, the TE injection resulted in a separate moderate focus of label in the head of the caudate, confirming Van Hoesen et al. (J. Comp. Neurol., '81, 199:205–219). Both retrograde and anterograde label was found in a number of subcortical sites. Labeled cells were found in the lateral basal nucleus of the amygdala, the substantia nigra pars compacta, the ventral tegmental area, and the parafascicular nucleus. The primary sites of anterograde label were the pars lateralis portion of the substantia nigra pars reticulata (SNr) and the caudal portions of the internal and external subdivisions of the globus pallidus (GP). Unlike the topographic arrangement of cortical inputs to the caudate, projections from distant portions of the tail and genu appeared to be highly convergent in both the SNr and GP. Because of the known projections from the lateral SNr to the superior colliculus and from the lateral SNr and caudal GP indirectly to prefrontal cortex, including the frontal eye field, the striatum may provide an important link in a visual pathway underlying oculomotor control and visuomotor associations.