Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos

Abstract

Posterior parietal cortex of prosimian galagos consists of a caudal half characterized by connections with visual cortex and a rostral half connected with motor, premotor, and visuomotor areas of frontal cortex. When 500-ms trains of electrical pulses were used to stimulate microelectrode sites throughout posterior parietal cortex, movements were elicited only from the rostral half. The movement zone reflected an overall pattern of somatotopy, from eye and face movements most ventrally to hindlimb movements most dorsally. In addition, subregions or zones of this movement cortex seemed to be devoted to components of different, ethologically significant behaviors. Thus, microstimulation within separate zones of cortex elicited reaching, hand-to-mouth, defensive, or aggressive movements. The finding of similar classes of elicited movement patterns from frontal and more recently intraparietal cortex of macaques suggests that multiareal circuits for biologically significant behaviors are components of all primate brains and that these circuits can be activated by long trains of current pulses at rostral locations in posterior parietal cortex.

Fig. 1.

Classes of movements evoked by microstimulation of different zones of rostral PPC of galagos. Each segment of drawing depicts first and last phases of a type of complex movement traced from video recordings. (A) The aggressive face pattern included a backward folding of the ear, a squint of the eye, and an opening of the mouth to expose the teeth. (B) The forelimb defensive movement included a positioning of the forelimb near the face with the palm out as if to ward off a blow. (C) The hand-to-mouth movement brought the grasping hand to or near the mouth. (D) The reaching movement was a reach in front of the galago with a grasp.

Fig. 2.

A summary of PPC organization in galagos based on present results. (A) A photograph of part of the exposed left cerebral hemisphere of a galago with functionally distinct movement zones outlined and colored. See Evoked Movement Patterns for descriptions of the movement patterns. The regions of anterior somatosensory cortex and motor cortex are indicated, and the intraparietal (IPS), lateral (LS), anterior frontal (FSa), and the posterior frontal (FSp) sulci are marked. (B) A dorsolateral view of galago brain with the area of interest shown in A in a box. Primary (V1), secondary (V2), and middle temporal (MT) visual areas, somatosensory areas S1 and 3a, primary motor cortex (M1), premotor cortex (PM), and FEF are labeled for reference. The superior temporal sulcus is apparent just ventral to MT. (C) A summary of patterns of projections revealed by injections of retrogradely transported tracers into PPC. Injections of tracers into the caudal half of PPC labeled neurons in visual areas, including MT, DL (the dorsolateral area), the dorsomedial area, V3, and V2. White arrows indicate projections from these fields. Injections in the rostral PPC labeled different areas. Injections into the ventral part of this rostral zone labeled neurons in some non-primary visual areas, secondary somatosensory fields, ventral motor and premotor cortex, and the FEF (yellow arrows). Injections into the dorsal part of this rostral zone labeled neurons in secondary somatosensory fields, middle motor cortex, and dorsal premotor cortex (green arrows).

Fig. 3.

The organization of PPC in galago 04-04. (A) A dorsolateral view of the exposed part of the left cerebral hemisphere with microstimulation sites marked by dots. The numbered small black dots to the left (rostral) were stimulated by 60-ms trains to produce simple movements that allowed us to locate motor and somatosensory cortex for reference. The 500-ms trains of pulses were used elsewhere. The most caudal stimulation sites (white dots) failed to produce movements. Other locations produced complex movements as indicated by the color code for dots. Sites outside the marked movement zones were excluded on the basis of quality of movement and movement thresholds. Occasionally, the long stimulus trains produced only a simple movement, usually of the ear (large black dots). The number beneath each dot indicates threshold current levels for complex movements in μA. Dorsal PPC represented complex forelimb movements (defensive, hand-to-mouth, and reaching), whereas ventral PPC represented complex face movements (defensive and aggressive). The dorsomedial portion of PPC was devoted to both forelimb and hindlimb movements, with most sites producing bilateral movements (bi). Movements of specific body parts are coded as follows: E, ear; F, face; Fl, forelimb; and Hl, hindlimb. Dashed lines outline the posterior frontal sulcus (FSp), the intraparietal sulcus (IPS), and the lateral sulcus (LS). (B) Stimulation sites in cortex of the upper (Upper) and lower (Lower) banks of the IPS. Electrode penetration locations are marked on the brain surface with dots as in A. Vertical lines mark the projections of the penetrations onto the cortical surface in the sulcus, with horizontal bars indicating 200-μm steps where microstimulation occurred. The colored bars along penetrations illustrate the response type at each depth. No response was noted at uncolored depths.

Fig. 4.

The organization of PPC in galago 04-07. Conventions follow those of Fig. 3. (A) A dorsolateral view of the exposed portion of the left cerebral hemisphere with dots indicating the locations of electrode penetrations for microstimulation. Function zones for aggressive face and aggressive face with forearm movements (purple), defensive face (yellow), defensive forelimb (green), hand-to-mouth (dark blue), and hindlimb (gray) movements are outlined. No separate reaching zone was found in this case, whereas an eye movement zone (orange) was noted. (B) Results from penetrations where sites along the upper (Upper) and lower (Lower) banks of the intraparietal sulcus were stimulated.