Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

Abstract

In primates, lesions of striate cortex (V1) result in scotomas in which only rudimentary visual abilities remain. These aspects of vision that survive V1 lesions have been attributed to direct thalamic pathways to extrastriate areas, including the middle temporal area (MT). However, studies in New World monkeys and humans have questioned this interpretation, suggesting that remnants of V1 are responsible for both the activation of MT and residual vision. We studied the visual responses of neurons in area MT in New World marmoset monkeys in the weeks after lesions of V1. The extent of the scotoma in each case was estimated by mapping the receptive fields of cells located near the lesion border and by histological reconstruction. Two response types were observed among the cells located in the part of MT that corresponds, in visuotopic coordinates, to the lesioned part of V1. Many neurons (62%) had receptive fields that were displaced relative to their expected location, so that they represented the visual field immediately surrounding the scotoma. This may be a consequence of a process analogous to the reorganization of the V1 map after retinal lesions. However, another 20% of the cells had receptive fields centered inside the scotoma. Most of these neurons were strongly directionselective, similar to normal MT cells. These results show that MT cells differ in their responses to lesioning of V1 and that only a subpopulation of MT neurons can be reasonably linked to residual vision and blindsight.

Responses of Neurons in the Middle Temporal Visual Area After Long-Standing Lesions of the Primary Visual Cortex in Adult New World Monkeys

“…In contrast, Rosa et al (2000) concluded from recordings weeks after V1 lesions in marmosets that many neurons (at least 31%) in the deprived portions of MT had receptive fields displaced from predicted locations so that they responded to stimuli activating intact portions of V1. Thus, there was evidence for considerable retinotopic reorganization of MT.…”

“…However, the remaining 18% of the sites within deprived MT encountered neurons that were spontaneously active but failed to respond to visual stimuli. In addition, given uncertainties about the sizes of the scotomas, Rosa et al (2000) stated that only 13 neurons "unequivocally responded to stimulation restricted to the scotoma." As in the experiments on owl monkeys, many neurons in deprived MT of marmosets were rendered unresponsive to visual stimuli, and others responded to stimuli activating intact portions of V1, yet 13 neurons appeared to be activated by a source of input that was independent of V1.…”

“…Because Rosa et al (2000) studied MT neurons weeks after V1 lesions, they suggested that total deactivation obtained immediately after the lesions by Kaas and Krubitzer (1992) could be attributable to a widespread depression that might follow a lesion (Seitz et al, 1999). This explanation seems unlikely, given that there were normal responses in portions of MT outside the deprived zone in the study of Kaas and Krubitzer (1992).…”

“…Recordings from one owl monkey (99-82) were obtained under gas anesthesia using halothane (0.8 -2.0%) while ventilating the animal with a 2:1 mixture of nitrous oxide and oxygen, as in a study by Girard et al (1992). Recordings were made from one additional owl monkey (00-54) under Sufenta anesthesia (12-15 g ⅐ kg Ϫ1 ⅐ hr Ϫ1 ; sufentanil citrate injection; Baxter Health Care Corporation, Deerfield, IL), as in studies by Rodman et al (1989) and Rosa et al (2000). The Sufenta was infused at a rate of 2.5-3.2 ml/hr in a mixture including vecuronium bromide (Norcuron; 0.1-0.2 mg ⅐ kg Ϫ1 ⅐ hr Ϫ1 ), 50% dextrose, and lactated Ringer's solution.…”

“…Because neurons in MT failed to respond to visual stimuli in monkeys with both V1 and superior colliculus (SC) lesions, a relay of visual information from the SC to the pulvinar and then to extrastriate cortex was postulated as the source of the visual activation of MT in the absence of V1 (Rodman et al, 1990). More recently, Rosa et al (2000) reported that V1 lesions in New World marmoset monkeys failed to completely deactivate neurons in MT.…”