Cortical visual area CSv as a cingulate motor area: a sensorimotor interface for the control of locomotion

The response properties, connectivity and function of the cingulate sulcus visual area (CSv) are reviewed. Cortical area CSv has been identified in both human and macaque brains. It has similar response properties and connectivity in the two species. It is situated bilaterally in the cingulate sulcus close to an established group of medial motor/premotor areas. It has strong connectivity with these areas, particularly the cingulate motor areas and the supplementary motor area, suggesting that it is involved in motor control. CSv is active during visual stimulation but only if that stimulation is indicative of self-motion. It is also active during vestibular stimulation and connectivity data suggest that it receives proprioceptive input. Connectivity with topographically organized somatosensory and motor regions strongly emphasizes the legs over the arms. Together these properties suggest that CSv provides a key interface between the sensory and motor systems in the control of locomotion. It is likely that its role involves online control and adjustment of ongoing locomotory movements, including obstacle avoidance and maintaining the intended trajectory. It is proposed that CSv is best seen as part of the cingulate motor complex. In the human case, a modification of the influential scheme of Picard and Strick (Picard and Strick, Cereb Cortex 6:342–353, 1996) is proposed to reflect this.

Afferent connections of cytoarchitectural area 6M and surrounding cortex in the marmoset: putative homologues of the supplementary and pre-supplementary motor areas

Cortical projections to the caudomedial frontal cortex were studied using retrograde tracers in marmosets. We tested the hypothesis that cytoarchitectural area 6M includes homologues of the supplementary and pre-supplementary motor areas (SMA and preSMA) of other primates. We found that, irrespective of the injection sites' location within 6M, over half of the labeled neurons were located in motor and premotor areas. Other connections originated in prefrontal area 8b, ventral anterior and posterior cingulate areas, somatosensory areas (3a and 1-2), and areas on the rostral aspect of the dorsal posterior parietal cortex. Although the origin of afferents was similar, injections in rostral 6M received higher percentages of prefrontal afferents, and fewer somatosensory afferents, compared to caudal injections, compatible with differentiation into SMA and preSMA. Injections rostral to 6M (area 8b) revealed a very different set of connections, with increased emphasis in prefrontal and posterior cingulate afferents, and fewer parietal afferents. The connections of 6M were also quantitatively different from those of M1, dorsal premotor areas, and cingulate motor area 24d. These results show that the cortical motor control circuit is conserved in simian primates, indicating that marmosets can be valuable models for studying movement planning and control.

Reward activations and face fields in monkey cingulate motor areas

Several premotor areas have been identified within primate cingulate cortex; however their function is yet to be uncovered. Recent brain imaging work in humans revealed a topographic anatomofunctional overlap between feedback processing during exploratory behaviors and the corresponding body fields in the rostral cingulate motor area (RCZa), suggesting an embodied representation of feedback. In particular, a face field in RCZa processes juice feedback. Here we tested an extension of the embodied principle in which unexpected or relevant information obtained through the eye or the face would be processed by face fields in cingulate motor areas, and whether this applied to monkey cingulate cortex. We show that activations for juice reward, eye movement, eye blink, and tactile stimulation on the face overlap over two subfields within the cingulate sulcus likely corresponding to the rostral and caudal cingulate motor areas. This suggests that in monkeys as is the case in humans, behaviorally relevant information is processed through multiple cingulate body/effector maps. NEW & NOTEWORTHY What is the role of cingulate motor areas? In this study we observed in monkeys that, as in humans, neural responses to face-related events, juice reward, eye movement, eye blink, and tactile stimulations, clustered redundantly in two separate cingulate subfields. This suggests that behaviorally relevant information is processed by multiple cingulate effector maps. Importantly, this overlap supports the principle that the cingulate cortex processes feedback based on where it is experienced on the body.

Area- and band-specific representations of hand movements by local field potentials in caudal cingulate motor area and supplementary motor area of monkeys

The caudal cingulate motor area (CMAc) and the supplementary motor area (SMA) play important roles in movement execution. The present study examined the neural mechanisms underlying these roles by investigating local field potentials (LFPs) from these areas while monkeys pressed buttons with either their left or right hand. During hand movement, power increases in the high-gamma (80–120 Hz) and theta (3–8 Hz) bands and a power decrease in the beta (12–30 Hz) band were observed in both the CMAc and SMA. High-gamma and beta activity in the SMA predominantly represented contralateral hand movements, whereas activity in the CMAc preferentially represented movement of either hand. Theta activity in both brain regions most frequently reflected movement of either hand, but a contralateral hand bias was more evident in the SMA than in the CMAc. An analysis of the relationships of the laterality representations between the high-gamma and theta bands at each recording site revealed that, irrespective of the hand preference for the theta band, the high-gamma band in the SMA preferentially represented contralateral hand movement, whereas the high-gamma band in the CMAc represented movement of either hand. These findings suggest that the input-output relationships for ipsilateral and contralateral hand movements in the CMAc and SMA differ in terms of their functionality. The CMAc may transform the input signals representing general aspects of movement into commands to perform movements with either hand, whereas the SMA may transform the input signals into commands to perform movement with the contralateral hand.

Distinct neuronal organizations of the caudal cingulate motor area and supplementary motor area in monkeys for ipsilateral and contralateral hand movements

The caudal cingulate motor area (CMAc) and the supplementary motor area (SMA) play important roles in movement execution. The present study aimed to characterize the functional organization of these regions during movement by investigating laterality representations in the CMAc and SMA of monkeys via an examination of neuronal activity during a button press movement with either the right or left hand. Three types of movement-related neuronal activity were observed: 1) with only the contralateral hand, 2) with only the ipsilateral hand, and 3) with either hand. Neurons in the CMAc represented contralateral and ipsilateral hand movements to the same degree, whereas neuronal representations in the SMA were biased toward contralateral hand movement. Furthermore, recording neuronal activities using a linear-array multicontact electrode with 24 contacts spaced 150 μm apart allowed us to analyze the spatial distribution of neurons exhibiting particular hand preferences at the submillimeter scale. The CMAc and SMA displayed distinct microarchitectural organizations. The contralateral, ipsilateral, and bilateral CMAc neurons were distributed homogeneously, whereas SMA neurons exhibiting identical hand preferences tended to cluster. These findings indicate that the CMAc, which is functionally organized in a less structured manner than the SMA is, controls contralateral and ipsilateral hand movements in a counterbalanced fashion, whereas the SMA, which is more structured, preferentially controls contralateral hand movements.

Comparison of abstract decision encoding in the monkey prefrontal cortex, the presupplementary, and cingulate motor areas

Deciding between alternatives is a critical element of flexible behavior. Perceptual decisions have been studied extensively in an action-based framework. Recently, we have shown that abstract perceptual decisions are encoded in prefrontal cortex (PFC) neurons ( Merten and Nieder 2012 ). However, the role of other frontal cortex areas remained elusive. Here, we trained monkeys to perform a rule-based visual detection task that disentangled abstract perceptual decisions from motor preparation. We recorded the single-neuron activity in the presupplementary (preSMA) and the rostral part of the cingulate motor area (CMAr) and compared it to the results previously found in the PFC. Neurons in both areas traditionally identified with motor planning process the abstract decision independently of any motor preparatory activity by similar mechanisms as the PFC. A larger proportion of decision neurons and a higher strength of decision encoding was found in the preSMA than in the PFC. Neurons in both areas reliably predicted the monkeys' decisions. The fraction of CMAr decision neurons and their strength of the decision encoding were comparable to the PFC. Our findings highlight the role of both preSMA and CMAr in abstract cognitive processing and emphasize that both frontal areas encode decisions prior to the preparation of a motor output.

The neural correlates of self-paced finger tapping in bipolar depression with motor retardation

ObjectiveMotor retardation is a characteristic feature of bipolar depression, and is also a core feature of Parkinson's disease. Within the framework of the functional deafferentiation theory in Parkinson's disease, we hypothesised that motor retardation in bipolar depression is mediated by disrupted subcortical activation, leading to decreased activation of cortical motor areas during finger tapping.MethodsWe used functional magnetic resonance imaging to investigate neural activity during self-paced finger tapping to elucidate whether brain regions that mediate preparation, control and execution of movement are activated differently in subjects with bipolar depression (n = 9) compared to healthy controls (n = 12).ResultsAn uncorrected whole-brain analysis revealed significant group differences in dorsolateral and ventromedial prefrontal cortex. Corrected analyses showed non-significant differences in patients compared to controls: decreased and less widespread activation of the left putamen and left pallidum; increased activity in the left thalamus and supplementary motor area; decreased activation in the left lateral pre- and primary motor cortices; absence of activation in the pre-supplementary motor area; activation of the bilateral rostral cingulate motor area.ConclusionBoth movement preparation and execution may be affected in motor retardation, and the activity in the whole left-side motor circuit is altered during self-initiated motor performance in bipolar depression.