Optical imaging in galagos reveals parietal-frontal circuits underlying motor behavior

Abstract

The posterior parietal cortex (PPC) of monkeys and prosimian galagos contains a number of subregions where complex, behaviorally meaningful movements, such as reaching, grasping, and body defense, can be evoked by electrical stimulation with long trains of electrical pulses through microelectrodes. Shorter trains of pulses evoke no or simple movements. One possibility for the difference in effectiveness of intracortical microstimulation is that long trains activate much larger regions of the brain. Here, we show that long-train stimulation of PPC does not activate widespread regions of frontal motor and premotor cortex but instead, produces focal, somatotopically appropriate activations of frontal motor and premotor cortex. Shorter stimulation trains activate the same frontal foci but less strongly, showing that longer stimulus trains do not produce less specification. Because the activated sites in frontal cortex correspond to the locations of direct parietal-frontal anatomical connections from the stimulated PPC subregions, the results show the usefulness of optical imaging in conjunction with electrical stimulation in showing functional pathways between nodes in behavior-specific cortical networks. Thus, long-train stimulation is effective in evoking ethologically relevant sequences of movements by activating nodes in a cortical network for a behaviorally relevant period rather than spreading activation in a nonspecific manner.

Fig. 1.

Summary of the PPC organization in galago. Functionally distinct movement zones are marked with colors on the exposed left hemisphere. Connections between functional PPC zones and frontal motor region PM-M1 are marked with color-coordinated arrows. This view matches the location of Inset on the schematic of PPC functional zones on a dorsolateral view of the hemisphere (lower right corner). Black dashed lines mark approximate borders of M1 and the border between rostral (PPCr) and caudal PPC (PPCc). The dotted line marks the border between the M1 forelimb and face representations. M1, primary motor cortex; PMD and PMV, dorsal and ventral motor areas; PPCr and PPCc, rostral and caudal posterior parietal cortex; FSa and FSp, anterior and posterior frontal sulci; IPS, intraparietal sulcus; LS, lateral sulcus; FEF, frontal eye field; DL, dorsolateral visual area; MT, middle temporal area; S1, primary somatosensory area; V1, primary visual area; V2, secondary visual area. (Scale bar: 1 mm.)

Fig. 2.

Intrinsic cortical activity in response to electrical stimulation of PPC in galago 08-08. Electrical stimulation (300-μA, 500-ms train) of the face region of ventral PPC evoked a face defensive movement. (A) Pattern of blood vessels on the exposed brain surface. Green rectangle marks imaged M1-PM field. Green dot 8 in face representation of PPC indicates the site of electrical stimulation for illustrated cortical activation. Gray dots mark other stimulation sites. Dashed lines indicate approximate borders of M1, and the dotted line indicates the border between the forelimb and face M1 representations. (B) Intrinsic response (dark region) temporally averaged 1–2 s after stimulus onset. (C) Blank response during the no stimulus condition. (D) Image maps showing time course of activation after stimulation onset. Frame duration is 200 ms. The first frame is the corresponding blood vessel map of images. Activations in M1 and PMV are indicated with pink and yellow arrows, respectively. (E) Time course of changes in reflectance from three regions of interest centered over (Left) M1 (pink box in B), (Center) M1/PMV (yellow box in B), and (Right) dorsal M1 (blue box in B) in trials with electrical stimulation (colored lines) and blank trials (black lines). Stimulation period is indicated by green bars in D and E. Error bars = SD. (Scale bar: 1 mm.) A, anterior; M, medial; L, lateral; P, posterior. Imaged left cortex from 18 trials.

Fig. 3.

Time course of cortical activation from an individual trial in case 08-08 (compare with Fig. 2). The top left frame shows a photograph of the imaged cortex. Subsequent frames correspond to a sequence of 200-ms imaging times from a single trial. The black bar represents the stimulus. (Scale bar: 1 mm.)

Fig. 4.

Maps of activation evoked by electrical stimulation of PPC in galago 08-18. Electrical stimulation of PPC (300- to 400-μA, 500-ms trains) that evokes face (A) and arm (B) behaviors produces topographical activation of the M1-PM cortex, which is revealed by intrinsic optical imaging of the hemodynamic response. (C) Activity maps (4–12) recorded for face and forelimb movements. Evoked face movements: 4, defensive face (+ mouth opens); 10, defensive face. Evoked forelimb movements: 6, forward reach; 7, forward reach, 8, slight arm lift + ear; 9, lateral outward reach; 12, arm lift. Stimulation of 11 (face region) did not evoke any movement. For clarity, each intrinsic optical imaging map is paired with a t-test map of cortical motor activity after filtering out random occurring pixels and small clusters of pixels. The t-test map for 11 is presented without filtering to illustrate the level of random significant pixels. White dotted lines in t-test maps mark the borders between forelimb and face representations. Green dots on the dorsolateral view of the exposed cortical surface (C Middle Center) mark the stimulation sites for shown activation maps. Gray dots mark other stimulated sites. Red stars mark lesions. (Scale bar: 5 mm.) Other conventions are as in Figs. 1 and 2.

Fig. 5.

Areas of activation elicited by electrical stimulation of PPC in case 08-18. (A) Photomicrograph of exposed cortical surface shows the pattern of blood vessels with the marked M1-PM imaged region (green rectangle) and sites of stimulation in PPC (green dots). (B) Reconstructions of the left brain hemisphere shown on the flattened view with stimulated sites (green dots) and areal borders approximated from CO and myelin sections. The green rectangle marks the imaged field. (C) Areas of activation overlaid on a blood vessels map. Stimulus amplitudes were 300–400 μA. Areas activated during face movements were observed laterally, and areas activated during forelimb movements were observed medially. (Scale bars: A and B, 5 mm; C, 1 mm.) Other conventions are the same as in Figs. 1 and 2.

Fig. 6.

Intrinsic motor cortex activity to different durations of electrical stimulation of PPC in case 08-18. Electrical stimulation (400 μA) of the dorsal PPC (green dot 9 in H) evoked a lateral reaching movement. (A–D) Optical imaging maps and (E–G) t-test maps of motor cortical activity to 500- (A and E), 120- (B and F), and 60-ms (C and G) duration of stimulus. (D) Image map for the no stimulus blank condition. (H) Blood vessels image shows imaged frontal M1-PM region (green rectangle) with site of stimulation in PPC (green dot 9). (I) Change in reflectance for a region of interest (pink square in A) vs. time for different stimulus train durations to stimulation at site 9. (J) Peak percent change in reflectance to 500-, 120-, and 60-ms stimulation for six different sites of stimulation. (K) Area of activation as measured by the number of significant pixels (P < 0.01, uncorrected) to 500-, 120-, and 60-ms stimulation for six different sites of stimulation. *P < 0.01, 500 ms > 120 ms, 500 ms > 60 ms. Clip value = 0.05%. (Scale bars: A–G, 1 mm; H, 5 mm.) Other conventions are the same as in Fig. 2.

Fig. P1.

Parietal–frontal nodes in networks for reaching (blue) and face defensive (yellow) movements on a brain of prosimian primate (Otolemur garnetti). Dots in the blue region in PPC mark microelectrode penetrations where electrical stimulation evoked reaching movements and activated groups of neurons in parts of dorsal premotor (PMD) and primary motor (M1) cortex (blue oval), which was revealed by optical imaging. Stimulation of more lateral sites in the face defensive zone (yellow) of PPC evoked a grimace and closing of the eye and activated regions within a more lateral zone of frontal cortex (yellow oval), including parts of ventral premotor cortex (PMV) and the face sector of M1. The supplementary motor area (SMA), subdivisions of somatosensory cortex (3a, S1, 1–2, PV, and S2), auditory cortex, and visual areas (V1, V2, V3, DM, MT, and MST) are outlined. IPS, the intraparietal sulcus; STS, superior temporal sulcus; LS, lateral sulcus.