Activation of parieto-frontal stream during reaching and grasping studied by positron emission tomography in monkeys

Abstract

The whole brain activation during visually guided reaching and grasping behaviors was investigated in three macaque monkeys using positron emission tomography (PET) scanning with [¹⁵O]H₂O. Activation was consistently observed in the parietal regions such as PO, MIP, VIP, LIP and AIP, frontal regions such as PMd, M1 and S1 on the contralateral hemisphere and in the ipsilateral intermediate and lateral deep cerebellar nuclei. Activation was also observed in the areas representing the central and peripheral visual field in the early visual cortices. Thus, the visuo-motor processing, including parieto-frontal stream, involved in the control of visually guided reaching and grasping behaviors could be visualized for the first time in macaque monkeys.

Introduction

Visually guided reaching and grasping are typical goal directed movements in which visual information about the spatial location and shape of the target object is processed for generation of sequentially coordinated multi-joint movements of the hand and arm (Arbib et al., 1985, Jeannerod, 1988). Many studies have been conducted to search for the neuroanatomical substrate of the visuo-motor processing underlying the control of reaching and grasping. In general, visual information leaves the primary visual cortex via two major pathways; a dorsal pathway directed to the posterior parietal cortex and the ventral one to the inferior temporal lobe (Ungerleider and Mishkin, 1982). Among these, the dorsal visual stream was supposed to be involved in the control of visually guided reaching and grasping because of existence of direct connection from the posterior parietal cortex to premotor frontal cortices (Milner and Goodale, 1995).

To understand the neural mechanism for the control of the reaching and grasping movements, it is essential to know the information carried by neurons in individual areas involved in the control and their relative contribution. There are a large number of descriptions on the neural activities of several cerebral cortical regions such as motor and premotor cortex (Caminiti et al., 1991, Wise et al., 1986, Foggassi et al., 1999, Gentilucci et al., 1988, Rizzolatti et al., 1988) and parietal cortex (Calton et al., 2002, Fattori et al., 2001, Taira et al., 1990, Sakata et al., 1995), and cerebellum (Fu et al., 1997, Greger et al., 2004, Kitazawa et al., 1998, van Kan et al., 1994) during the reaching and/or grasping tasks by electrophysiological recordings of single unit activities in non-human primates. However, in these studies, relative contribution of individual areas is not clear. Based on functional and anatomical studies, it has been proposed that reaching and grasping movements are controlled by separate pathways; reaching by a medial parieto-frontal pathway that involves medial bank of the intraparietal sulcus (IPS) and dorsal premotor cortex (PMd) and grasping by a lateral parieto-frontal stream involving the lateral bank of the IPS and ventral premotor cortex (PMv) (Jeannerod et al., 1995, Wise et al., 1997). However, several authors argue against the existence of these parallel visuo-motor channels (Desmurget et al., 1996, Mon-Williams and McIntosh, 2000). On the other hand, there is disagreement on the contribution of supplementary motor area (SMA) to simple visually guided reaching task (Picard and Strick, 2003). To obtain clearer perspective on these issues, we performed the brain activation studies in macaque monkeys while they are performing simple visually guided reaching and grasping task by measuring the cerebral blood flow (CBF) with PET scanning with [¹⁵O]H₂O. The advantages of using PET for studying the whole brain activation during reaching and grasping are: (1) there is little technical constraints on behaviors of the animals that can be conducted in the scanner, compared to fMRI; they can perform large body movements such as reaching in the 3D space, grasping a particular object, and eat it, and (2) it is possible to conduct a large number of scanning sessions to obtain clear brain imaging data in individual animals, which is usually not possible in humans.

By using this technique, we could clarify the whole brain regions involved in the visuo-motor processing for the control of visually guided reaching and grasping task. The present results will surely supply solid base on understanding the neural control of reaching and grasping movements.