Naomi Hasegawa

Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey

The cingulate motor areas reside within regions lining the cingulate sulcus and are divided into rostral and caudal parts. Recent studies suggest that the rostral and caudal cingulate motor areas participate in distinct aspects of motor function: the former plays a role in higher‐order cognitive control of movements, whereas the latter is more directly involved in their execution. Here, we investigated the organization of cingulate motor areas inputs to the basal ganglia in the macaque monkey. Identified forelimb representations of the rostral and caudal cingulate motor areas were injected with different anterograde tracers and the distribution patterns of labelled terminals were analysed in the striatum and the subthalamic nucleus. Corticostriatal inputs from the rostral and caudal cingulate motor areas were located within the rostral striatum, with the highest density in the striatal cell bridges and the ventrolateral portions of the putamen, respectively. There was no substantial overlap between these input zones. Similarly, a certain segregation of input zones from the rostral and caudal cingulate motor areas occurred along the mediolateral axis of the subthalamic nucleus. It has also been revealed that corticostriatal and corticosubthalamic input zones from the rostral cingulate motor area considerably overlapped those from the presupplementary motor area, while the input zones from the caudal cingulate motor area displayed a large overlap with those from the primary motor cortex. The present results indicate that a parallel design underlies motor information processing in the cortico‐basal ganglia loop derived from the rostral and caudal cingulate motor areas.

Thalamocortical and intracortical connections of monkey cingulate motor areas

Although there has been an increasing interest in motor functions of the cingulate motor areas, data concerning their input organization are still limited. To address this issue, the patterns of thalamic and cortical inputs to the rostral (CMAr), dorsal (CMAd), and ventral (CMAv) cingulate motor areas were investigated in the macaque monkey. Tracer injections were made into identified forelimb representations of these areas, and the distributions of retrogradely labeled neurons were analyzed in the thalamus and the frontal cortex. The cells of origin of thalamocortical projections to the CMAr were located mainly in the parvicellular division of the ventroanterior nucleus and the oral division of the ventrolateral nucleus (VLo). On the other hand, the thalamocortical neurons to the CMAd/CMAv were distributed predominantly in the VLo and the oral division of the ventroposterolateral nucleus‐the caudal division of the ventrolateral nucleus. Additionally, many neurons in the intralaminar nuclear group were seen to project to the cingulate motor areas. Except for their well‐developed interconnections, the corticocortical projections to the CMAr and CMAd/CMAv were also distinctively preferential. Major inputs to the CMAr arose from the presupplementary motor area and the dorsal premotor cortex, whereas inputs to the CMAd/CMAv originated not only from these areas but also from the supplementary motor area and the primary motor cortex. The present results indicate that the CMAr and the caudal cingulate motor area (involving both the CMAd and the CMAv) are characterized by distinct patterns of thalamocortical and intracortical connections, reflecting their functional differences. J. Comp. Neurol. 462:121–138, 2003.

Spontaneous synchronization of arm motion between Japanese macaques

Humans show spontaneous synchronization of movements during social interactions; this coordination has been shown to facilitate smooth communication. Although human studies exploring spontaneous synchronization are increasing in number, little is known about this phenomenon in other species. In this study, we examined spontaneous behavioural synchronization between monkeys in a laboratory setting. Synchronization was quantified by changes in button-pressing behaviour while pairs of monkeys were facing one another. Synchronization between the monkeys was duly observed and it was participant-partner dependent. Further tests confirmed that the speed of button pressing changed to harmonic or sub-harmonic levels in relation to the partners speed. In addition, the visual information from the partner induced a higher degree of synchronization than auditory information. This study establishes advanced tasks for testing social coordination in monkeys, and illustrates ways in which monkeys coordinate their actions to establish synchronization.

Large-Scale Information Flow in Conscious and Unconscious States: an ECoG Study in Monkeys

Consciousness is an emergent property of the complex brain network. In order to understand how consciousness is constructed, neural interactions within this network must be elucidated. Previous studies have shown that specific neural interactions between the thalamus and frontoparietal cortices; frontal and parietal cortices; and parietal and temporal cortices are correlated with levels of consciousness. However, due to technical limitations, the network underlying consciousness has not been investigated in terms of large-scale interactions with high temporal and spectral resolution. In this study, we recorded neural activity with dense electrocorticogram (ECoG) arrays and used the spectral Granger causality to generate a more comprehensive network that relates to consciousness in monkeys. We found that neural interactions were significantly different between conscious and unconscious states in all combinations of cortical region pairs. Furthermore, the difference in neural interactions between conscious and unconscious states could be represented in 4 frequency-specific large-scale networks with unique interaction patterns: 2 networks were related to consciousness and showed peaks in alpha and beta bands, while the other 2 networks were related to unconsciousness and showed peaks in theta and gamma bands. Moreover, networks in the unconscious state were shared amongst 3 different unconscious conditions, which were induced either by ketamine and medetomidine, propofol, or sleep. Our results provide a novel picture that the difference between conscious and unconscious states is characterized by a switch in frequency-specific modes of large-scale communications across the entire cortex, rather than the cessation of interactions between specific cortical regions.

A modified microsyringe for extracellular recording of neuronal activity

We describe a modified Hamilton microsyringe that allows extracellular recording of neuronal activity and subsequent injections. It is assembled with a Hamilton removable needle and a syringe for injection, a Teflon-coated tungsten wire for recording, and polyimide tubing as a sheath. The device is inexpensive and easy to handle in anatomical and physiological experiments in awake monkeys.

A cortical motor region that represents the cutaneous back muscles in the macaque monkey

A cortical motor region that represented the cutaneous muscles on the back was identified on the medial wall of the frontal lobe in the macaque monkey. In this region, neurons responded to somatosensory stimuli such as light touch or squeezing of the back skin, and intracortical microstimulation elicited contraction of the back skin. Such a region was located primarily on the dorsal bank of the cingulate sulcus, corresponding to the dorsal cingulate motor area.

Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus

How the motor-related cortical areas modulate the activity of the output nuclei of the basal ganglia is an important issue for understanding the mechanisms of motor control by the basal ganglia. In the present study, by using awake monkeys, the polysynaptic effects of electrical stimulation in the forelimb regions of the primary motor and primary somatosensory cortices on the activity of globus pallidus (GP) neurons, especially mediated by the subthalamic nucleus (STN), have been characterized. Cortical stimulation induced an early, short-latency excitation followed by an inhibition and a late excitation in neurons of both the external and internal segments of the GP. It also induced an early, short-latency excitation followed by a late excitation and an inhibition in STN neurons. The early excitation in STN neurons preceded that in GP neurons. Blockade of STN neuronal activity by muscimol (GABA(A) receptor agonist) injection resulted in abolishment of both the early and late excitations evoked in GP neurons by cortical stimulation. At the same time, the spontaneous discharge rate of GP neurons decreased, pauses between the groups of spikes of GP neurons became prominent, and the firing pattern became regular. Injection of (+/-)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) [N-methyl-D-aspartate (NMDA) receptor antagonist], but not 1,2,3, 4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium [NBQX (non-NMDA receptor antagonist)], into the STN attenuated the early and late excitations in GP neurons, suggesting that cortico-subthalamic transmission is mediated mainly by NMDA receptors. Interference with the pallido-subthalamic transmission by bicuculline (GABA(A) receptor antagonist) injection into the STN made the inhibition distinct without affecting the early excitation. The present results indicate that the cortico-subthalamo-pallidal pathway conveys powerful excitatory effects from the motor-related cortical areas to the GP with shorter conduction time than the effects conveyed through the striatum.

Disturbance in Task Performance after Inhibition of Subthalamic Nucleus Neurons

The subthalamic nucleus (STN) has been believed to be a key structure of the basal ganglia in the control of voluntary limb movement (DeLong, 1990; Albin et al., 1989b; Kitai and Kita, 1987; Whittier and Mettler,1949). An experimental lesion in the STN in monkeys produces violent involuntary movements of the leg and arm (Hamada and DeLong, 1992a; Carpenter et al, 1950; Whittier and Mettler, 1949). In normal subjects, however, it is not convincing that the STN plays an important role in the control of limb movement. Firing characteristics of STN neurons were studied in normal behaving monkeys (DeLong et al., 1985; Georgopoulos et al., 1983). Activity of STN neurons increased during movement, but in the majority of neurons the increase in firing begins after onset of the limb EMG. The increase in activity of STN neurons seems too late to account for movement initiation (Georgopoulos et al.,1983). Experimental lesion of the STN in normal awake monkeys (Hamada and DeLong, 1992a) provides little evidence for a significant effect of STN inactivation on voluntary movement. These findings are difficult to reconcile with the view that the STN plays an important role in the control of voluntary limb movement.

A new method for quantifying the performance of EEG blind source separation algorithms by referencing a simultaneously recorded ECoG signal

Blind source separation (BSS) algorithms extract neural signals from electroencephalography (EEG) data. However, it is difficult to quantify source separation performance because there is no criterion to dissociate neural signals and noise in EEG signals. This study develops a method for evaluating BSS performance. The idea is neural signals in EEG can be estimated by comparison with simultaneously measured electrocorticography (ECoG). Because the ECoG electrodes cover the majority of the lateral cortical surface and should capture most of the original neural sources in the EEG signals. We measured real EEG and ECoG data and developed an algorithm for evaluating BSS performance. First, EEG signals are separated into EEG components using the BSS algorithm. Second, the EEG components are ranked using the correlation coefficients of the ECoG regression and the components are grouped into subsets based on their ranks. Third, canonical correlation analysis estimates how much information is shared between the subsets of the EEG components and the ECoG signals. We used our algorithm to compare the performance of BSS algorithms (PCA, AMUSE, SOBI, JADE, fastICA) via the EEG and ECoG data of anesthetized nonhuman primates. The results (Best case >JADE = fastICA >AMUSE = SOBI ≥ PCA >random separation) were common to the two subjects. To encourage the further development of better BSS algorithms, our EEG and ECoG data are available on our Web site (http://neurotycho.org/) as a common testing platform.

Unintentional Synchronization of Behavior in Japanese Monkeys

The human studies in perception and action in social context revealed that social interaction facilitated behavioral synchronization. To understand brain mechanisms for the synchronization in details, studies in animal model are required. However, little is known about the behavioral synchronization in animals. Here we examined an unintentionally synchronized behavior in monkeys. The unintentional synchronization was quantified by changes in button-pressing behavior while two monkeys were seated facing each other. Different experimental conditions were applied to explore interferences of visual information on the speed and the timing of the button-pressing. The changes in behavior were observed when the subject was paired with another monkey, suggesting that social bonds play an important role in synchronization through visuo-motor or auditory-motor coupling to other’s behaviors.