Segregated Pathways Carrying Frontally Derived Top-Down Signals to Visual Areas MT and V4 in Macaques

Abstract

The bottom-up processing of visual information is strongly influenced by top-down signals, at least part of which is thought to be conveyed from the frontal cortex through the frontal eye field (FEF) and the lateral intraparietal area (LIP). Here we investigated the architecture of multisynaptic pathways from the frontal cortex to the middle temporal area (MT) of the dorsal visual stream and visual area 4 (V4) of the ventral visual stream in macaques. In the first series of experiments, the retrograde trans-synaptic tracer, rabies virus, was injected into MT or V4. Three days after rabies injections, the second-order (disynaptically connected) neuron labeling appeared in the ventral part of area 46 (area 46v), along with the first-order (monosynaptically connected) neuron labeling in FEF and LIP. In the MT-injection case, second-order neurons were also observed in the supplementary eye field (SEF). In the next series of experiments, double injections of two fluorescent dyes, fast blue and diamidino yellow, were made into MT and V4 to examine whether the frontal inputs are mediated by distinct or common neuronal populations. Virtually no double-labeled neurons were observed in FEF or LIP, indicating that separate neuronal populations mediate the frontal inputs to MT and V4. The present results define that the multisynaptic frontal input to V4 arises primarily from area 46v, whereas the input to MT arises from not only area 46v but also SEF, through distinct FEF and LIP neurons. Segregated pathways from the frontal cortex possibly carry the functionally diverse top-down signals to each visual stream.

Unilateral Prefrontal Lesions Impair Memory-Guided Comparisons of Contralateral Visual Motion

“…Careful mapping revealed deficits across multiple locations of the contralesional hemifield, with the vertical meridian providing clear separation between the intact and reduced performance. This pattern of results points to the importance of connectivity between the LPFC and the retinotopically organized cortical areas that process contralateral visual stimuli within the same hemisphere (Barbas, 1988;Schall et al, 1995;Petrides and Pandya, 2006;Ninomiya et al, 2012). It is also consistent with reports of the preference in the prefrontal cortex for contralateral stimuli (Boch and Goldberg, 1989;Funahashi et al, 1989;Sakagami and Niki, 1994;Rainer et al, 1999;Everling et al, 2002).…”

“…Overall, the similarity in the pattern of deficits observed in the three monkeys and the involvement of area 8Av in their lesions suggests a role of this portion of prefrontal cortex in motion comparisons. In the context of our task, area 8Av is of particular interest because of its direct reciprocal connectivity with motion processing areas MT and MST (Petrides and Pandya, 2006;Ninomiya et al, 2012). Although in all animals the lesion extended into area 8Av, the damage to this area was less extensive in M123, and this monkey exhibited relatively modest deficits.…”

“…The lesions included regions anatomically connected to the motion processing areas MT and MST (Barbas, 1988;Petrides and Pandya, 2006;Ninomiya et al, 2012) and shown to be active during all stages of memory-guided motion comparison tasks (Zaksas and Pasternak, 2006;Hussar and Pasternak, 2009.…”

Visuomotor Functions in the Frontal Lobe

“…Area 12 borders areas 11 and 13, which occupy the orbitofrontal cortex. The rostral pole is area 10. project to visual area V4 and the medial temporal area (MT), and those projecting to V4 receive input from area 46v, whereas those projecting to MT receive input from both area 46v and the supplementary eye field (SEF) (Ninomiya et al 2012). Findings such as these contradict the hoary dictum that "everything is connected to everything" and should highlight the enormous gap between the low-resolution functional descriptions of various brain areas and the specificity and diversity of high-resolution anatomical descriptions.…”

“…These findings sharply limit the scope of the premotor theory of attention. Recall that V4 and MT (and likely LIP and MST, among others) are innervated by different neurons in L2/3 of the FEF, and these neurons themselves have qualitatively different afferents (Ninomiya et al 2012). Thus, the so-called top-down signals from the FEF to each extrastriate area likely convey functionally different influences.…”