Ipsilateral-Dominant Control of Limb Movements in Rodent Posterior Parietal Cortex

• Published in: The Journal of neuroscience 2019-01, Vol.39 (3), p.485-502
• Main Authors: Soma, Shogo, Yoshida, Junichi, Kato, Shigeki, Takahashi, Yukari, Nonomura, Satoshi, Sugimura, Yae K, Ríos, Alain, Kawabata, Masanori, Kobayashi, Kazuto, Kato, Fusao, Sakai, Yutaka, Isomura, Yoshikazu
• Format: Article
• Language: English
• Subjects: Activation; Animals; Channelrhodopsins - genetics; Channelrhodopsins - physiology; Conditioning, Operant; Cortex (frontal); Cortex (motor); Cortex (parietal); Electromyography; Firing pattern; Forelimb - physiology; Functional Laterality - physiology; gamma-Aminobutyric Acid - metabolism; gamma-Aminobutyric Acid - physiology; Homology; Inhibition; Male; Motor Cortex - physiology; Motors; Movement - physiology; Neural networks; Neurons; Optogenetics; Parietal Lobe - physiology; Patch-Clamp Techniques; Primates; Psychomotor Performance - physiology; Rats; Rats, Transgenic; Representations; Rodentia; Rodents; Thalamus; γ-Aminobutyric acid
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.1584-18.2018

It is well known that the posterior parietal cortex (PPC) and frontal motor cortices in primates preferentially control voluntary movements of contralateral limbs. The PPC of rats has been defined based on patterns of thalamic and cortical connectivity. The anatomical characteristics of this area suggest that it may be homologous to the PPC of primates. However, its functional roles in voluntary forelimb movements have not been well understood, particularly in the lateralization of motor limb representation; that is, the limb-specific activity representations for right and left forelimb movements. We examined functional spike activity of the PPC and two motor cortices, the primary motor cortex (M1) and the secondary motor cortex (M2), when head-fixed male rats performed right or left unilateral movements. Unlike primates, PPC neurons in rodents were found to preferentially represent ipsilateral forelimb movements, in contrast to the contralateral preference of M1 and M2 neurons. Consistent with these observations, optogenetic activation of PPC and motor cortices, respectively, evoked ipsilaterally and contralaterally biased forelimb movements. Finally, we examined the effects of optogenetic manipulation on task performance. PPC or M1 inhibition by optogenetic GABA release shifted the behavioral limb preference contralaterally or ipsilaterally, respectively. In addition, weak optogenetic PPC activation, which was insufficient to evoke motor responses by itself, shifted the preference ipsilaterally; although similar M1 activation showed no effects on task performance. These paradoxical observations suggest that the PPC plays evolutionarily different roles in forelimb control between primates and rodents. In rodents, the primary and secondary motor cortices (M1 and M2, respectively) are involved in voluntary movements with contralateral preference. However, it remains unclear whether and how the posterior parietal cortex (PPC) participates in controlling multiple limb movements. We recorded functional activity from these areas using a behavioral task to monitor movements of the right and left forelimbs separately. PPC neurons preferentially represented ipsilateral forelimb movements and optogenetic PPC activation evoked ipsilaterally biased forelimb movements. Optogenetic PPC inhibition via GABA release shifted the behavioral limb preference contralaterally during task performance, whereas weak optogenetic PPC activation, which was insufficient to evoke motor