Elsevier

Progress in Neurobiology

Volume 58, Issue 6, August 1999, Pages 473-540
Progress in Neurobiology

14C-Deoxyglucose mapping of the monkey brain during reaching to visual targets

https://doi.org/10.1016/S0301-0082(98)00080-XGet rights and content

Abstract

The strategies used by the macaca monkey brain in controlling the performance of a reaching movement to a visual target have been studied by the quantitative autoradiographic 14C-DG method.

Experiments on visually intact monkeys reaching to a visual target indicate that V1 and V2 convey visuomotor information to the cortex of the superior temporal and parietoccipital sulci which may encode the position of the moving forelimb, and to the cortex in the ventral part and lateral bank of the intraparietal sulcus which may encode the location of the visual target. The involvement of the medial bank of the intraparietal sulcus in proprioceptive guidance of movement is also suggested on the basis of the parallel metabolic effects estimated in this region and in the forelimb representations of the primary somatosensory and motor cortices. The network including the inferior postarcuate skeletomotor and prearcuate oculomotor cortical fields and the caudal periprincipal area 46 may participate in sensory-to-motor and oculomotor-to-skeletomotor transformations, in parallel with the medial and lateral intraparietal cortices.

Experiments on split brain monkeys reaching to visual targets revealed that reaching is always controlled by the hemisphere contralateral to the moving forelimb whether it is visually intact or `blind'. Two supplementary mechanisms compensate for the `blindness' of the hemisphere controlling the moving forelimb. First, the information about the location of the target is derived from head and eye movements and is sent to the `blind' hemisphere via inferior parietal cortical areas, while the information about the forelimb position is derived from proprioceptive mechanisms and is sent via the somatosensory and superior parietal cortices. Second, the cerebellar hemispheric extensions of vermian lobules V, VI and VIII, ipsilateral to the moving forelimb, combine visual and oculomotor information about the target position, relayed by the `seeing' cerebral hemisphere, with sensorimotor information concerning cortical intended and peripheral actual movements of the forelimb, and then send this integrated information back to the motor cortex of the `blind' hemisphere, thus enabling it to guide the contralateral forelimb to the target.

Introduction

The evolutionary value of goal-directed behavior in survival and phylogenetic selection is undisputable. At the lowest level, goal-directed behavior consists of a sensorimotor praxis, perception in conjunction with action. Visually guided reaching for reward is an elemental sensorimotor behavior which may be considered as isomorphic with a cognitive system. Unravelling the neural bases of sensorimotor behavior could provide tools to understanding higher brain functions. After all, interworking between mental and cerebral processes, between impressions of the mind which mirror the cosmos and our wish to comprehend their neural bases is a common, central theme in the fragmented field of neurosciences. Thus, our attempt to review the neural networks underlying visually guided reaching which have been identified by quantitative metabolic mapping at this window in time is justified.

Although sensation is processed bottom–up the sensory hierarchy and action is processed top–down the motor hierarchy, there is not a single place of integration of the visual perception or the motor praxis. Indeed, the dominant current neuroscientific ideology assumes that within the cerebral cortex, which is the last step of phylogenetic development, there are several areas contributing to the composition of a picture or of a motor command (Georgopoulos, 1986; Livingstone and Hubel, 1988; Moutoussis and Zeki, 1997a; Wise and Godschalk, 1987; Zeki, 1978). This body of ideas would predict functional activation in several visual and motor cortical areas during performance of a visually guided reaching task, without any high-order `master' area, order-dominant over all, displaying exceptionally high metabolic activity.

The syntactic code of the visually guided reaching behavior involves in theory:

  • 1.

    engagement of attention in the sense of orienting to locations of expected visual stimuli;

  • 2.

    perception of the visual stimulus in the extrapersonal space based on head position, gaze direction and retinal position of the target;

  • 3.

    transformation of signals about the extrapersonal location of the stimulus into an intrinsic coordinate system of central representation;

  • 4.

    selection of the oculomotor schema;

  • 5.

    execution of the eye-movement to the visual target;

  • 6.

    attention in terms of iconic detection of target qualities;

  • 7.

    selection of the skeletomotor schema;

  • 8.

    initiation and execution of the forelimb movement toward the visual target;

  • 9.

    constant interactions between visual input (concerning the target and forelimb locations), proprioceptive somatosensory input (concerning the forelimb configuration) and motor outflow during performance of the task; and

  • 10.

    attention in the sense of maintaining the alert state.

This description indicates the functional involvement of multiple sensory, motor, uni-, bi- and polymodal association cortical brain areas, as well as the cortical regions related with motivation, intention, reward, active working-memory processes, and the different aspects of attention during the performance of the visually guided reaching task.

The strategies used by the brain in controlling the performance of visually guided movements must be governed by the fact that perception of: (i) the alternatively illuminated visual cues (start and target keys); and (ii) the moving forelimb toward the keys constitutes a complex system of relations, with the external phenomena under constant modification rather than static, demanding updating of the sensory equilibrium and accommodation to new phenomena. The subject has to take into account the temporal and spatial attributes of the percepts simultaneously with the temporal and spatial dimensions of its oculomotor and skeletomotor acts. Every single moment, the subject's perception is influenced by its motor activity just as the latter is influenced by the former. Sensory inflow shapes the movement, which in turn shapes the dynamic patterns of sensory input and data acquisition. This prerequisite for simultaneous perceptual and motor assimilation indicates that the motor act is inseparable from the sensory percept, and that polymodal cortical areas involved in multisensory and motor convergence may be activated.

The progress in revealing the neuronal machinery underlying visually guided reaching has been gradual and incremental. This progress is based on the results of neuroanatomical tracing, lesion, single unit recording, imaging and psychophysical studies which indicate the functional involvement of a few discrete cerebral neocortical areas. These areas involve the primary motor area 4 (Caminiti et al., 1990; Georgopoulos et al., 1982; Schwartz et al., 1988), the premotor lateral area 6 and the supplementary motor area (SMA) (Caminiti et al., 1991; Halsband and Passingham, 1982; Rizzolatti et al., 1987; Sasaki and Gemba, 1986; Tanji and Kurata, 1985; Weinrich and Wise, 1982), as well as the posterior parietal areas 5 and 7 (Georgopoulos and Massey, 1985; Halsband and Passingham, 1982; Kalaska et al., 1983; Mountcastle et al., 1975; Sakata et al., 1995; Taira et al., 1990). However, evidence exists for several arm–hand motor cortical areas in each hemisphere (Barbas and Pandya, 1987; Freund, 1991; Luppino et al., 1991; Matelli et al., 1986), for several cortical areas related to eye-movements (Andersen, 1995; Bruce et al., 1985; Schlag and Schlag-Rey, 1987), for many visual cortical areas encoding spatial or iconic categories (Colby and Duhamel, 1991; Ungerleider and Mishkin, 1982; Van Essen et al., 1992; Zeki and Shipp, 1988; Zeki, 1978) and for several arm–hand somatosensory cortical areas (Kaas et al., 1979; Pearson and Powell, 1985; Robinson and Burton, 1980b; Sakata, 1975). Given that the sensory and motor systems are endowed with several serial, parallel and reciprocal pathways, a complex scenario of activations during the performance of visually guided reaching movements emerges. This scenario predicts the activation of a plethora of visual, somatosensory, oculomotor, skeletomotor and association cortical regions related with the attentive, perceptual, and motor categories involved in the task.

In conclusion, we would foresee massive involvement of brain areas, due to many independent modular brain systems which function together for the reconstruction of an order behind the seeming complexity, towards the emergence of efficient sensorimotor behavior. Indeed, our recent metabolic mapping studies using the 14C-deoxyglucose (14C-DG) quantitative autoradiographic method demonstrate the functional involvement of several cortical and subcortical regions of the monkey brain during performance of visually guided reaching movements (Dalezios et al., 1996; Savaki et al., 1993, Savaki et al., 1996, Savaki et al., 1997). The 14C-DG quantitative method (Sokoloff et al., 1977) provides the blessing or the anathema of mapping the metabolic activity within all brain structures simultaneously. There are two traditional ways of presenting the 14C-DG generated quantitative imaging data. The first way involves presentation of selected results in specific regions based on pathways expected to be associated with the behavior under investigation. However, the word `data' means given results rather than taken out of a pool of findings according to our expectations and our convenience. Thus we intentionally use the second way of presentation of imaging data that involves a sweeping report. We illustrate at present all the activated cortical areas, which include the striate and prestriate cortices, the inferior intraparietal and superior temporal visual association areas, the frontal eye field (FEF) and the caudal periprincipal cortex, the primary somatosensory and the related superior intraparietal area, the primary and association auditory cortices, the superior temporal multimodal region, and the premotor, the primary, SMA and cingulate motor areas (CMA). The activated subcortical areas involve thalamic and pontine nuclei as well as paravermal and lateral hemispheric cerebellar regions. The different pathways activated in the visually intact and in the split-brain monkeys indicate distinct strategies used by the `seeing' and the `blind' hemispheres in control of the forelimb movements.

Section snippets

Visually intact monkeys

Three visually intact adult female Macaca nemestrina monkeys have been used in this series of experiments. The first was trained to perform the visually guided reaching task with its right forelimb, the second was trained to perform the same task with its left forelimb, and the third monkey was an untrained normal control seated in front of the non-functioning test panel and receiving neither visual stimuli nor liquid reward during the 14C-DG experiment.

The test panel in front of the monkey

Split brain monkeys

Seven rhesus monkeys (M. mulatta) have been used in this series of experiments. Two of these monkeys were normal controls, two had transection of the right optic tract, and three had right optic tract section combined with transection of the corpus callosum and of the hippocampal and anterior commissures. The latter procedure (optic tract section plus forebrain commissurotomy) deprived the right hemisphere of all known visual input (Savaki et al., 1993).

The monkeys were trained to perform a

Acknowledgements

The experiments on monkeys reported in the present review were designed, performed or analyzed in collaboration with Charles Kennedy, Mortimer Mishkin and Louis Sokoloff at NIH (Bethesda-Maryland), Roberto Caminiti at the University of `Sapienza' (Rome-Italy), and with Vassilis Raos and Georgia Gregoriou at the University of Crete (Iraklion-Greece). These experiments were supported by grants of: the European Community Human Capital and Mobility ERBCHRXCT 930266 and ERBCHBGCT920085; the Greek

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