Distant heterotopic callosal connections to premotor cortex in non-human primates

Abstract

Abstract-Cortico-cortical connectivity has become a major focus of neuroscience in the last decade but most of the connectivity studies focused on intrahemispheric circuits. Little has been reported about information acquired and processed in the premotor cortex and its functional connection with its homotopic counterpart in the opposite hemisphere via the corpus callosum. In non-human primates (macaques) lateralization is not well documented and its exact role is still unknown. The present study confirms in two macaques the existence of homotopic contralateral projections and completes the picture by further exploring heterotopic (non-motor) callosal projections. This was tested by injecting retrograde tracers in the premotor cortical areas PMv and PMd (targets). Our method consisted of identifying the connections with all the homo-and heterotopic cortical areas located in the contralateral hemisphere. The results showed that PMd and PMv receive multiple low-density labeled inputs from the opposite heterotopic prefrontal, parietal, motor, insular and temporal regions. Such unexpected collection of transcallosal inputs from heterotopic areas suggests that the premotor areas communicate with other modalities through long distance low-density networks which could have important implications in the understanding of sensorimotor and multimodal integration.

Mapping effective connectivity between the frontal and contralateral primary motor cortex using dual-coil transcranial magnetic stimulation

“…For instance, Rouiller et al (1994) found that cM1 receives approximately 50% of its inputs from the premotor cortex; these are mainly found in an area close to our area 6d/FEF region. Other studies show that there are dense homotopic and heterotopic callosal connections between the right and left dorsal and ventral PM, with sparse heterotopic connections from other motor and non-motor regions (Boussaoud et al, 2005;Lanz et al, 2017). This provides the current study with two main possible pathways for the net cM1 output, namely iPM -cM1 or iPM -cPM -cM1.…”

“…iPM -iM1 -cM1). Alternatively, PM transcallosal projections could also transfer this information to the cM1 (Boussaoud et al, 2005;Lanz et al, 2017;Marconi et al, 2003;Rouiller et al, 1994). For instance, Rouiller et al (1994) found that cM1 receives approximately 50% of its inputs from the premotor cortex; these are mainly found in an area close to our area 6d/FEF region.…”

“…Alternatively, information concerning action choice could be relayed from DLPFC to cPMd then to cM1, since some monkey studies show strong projections from the prefrontal cortex to cPMd (Boussaoud et al, 2005). Though other contralateral DLPFC and PM projections are somewhat sparser, the number of labelled projections are non-negligible and thus still probably functionally relevant (Lanz et al, 2017;Marconi et al, 2003). Despite the route, it is clear that stimulation of the area affects net contralateral motor output in a task-dependent manner.…”

“…The primary motor cortex (M1) and frontal regions of the brain can be distinguished by their cyto-, myelo-, receptor-based architecture and complex array of connections between each other, and other parts of the cortex (Amunts and Zilles, 2015;Fan et al, 2016;Glasser et al, 2016;Luppino and Rizzolatti, 2000;Pandya, 1999, 2002). Anatomical studies have demonstrated that neurons in frontal areas project to M1 both ipsilaterally Strick, 1991, 2002;Luppino and Rizzolatti, 2000) and contralaterally, via the corpus callosum (Boussaoud et al, 2005;Fang et al, 2008;Lanz et al, 2017;Marconi et al, 2003). Information provided by these connections to M1 help shape motor commands for voluntary movements such as grasping and manipulating objects.…”

“…Neuroanatomical tracing techniques in the monkey have revealed that each premotor area has a specific pattern of connections (Dum and Strick, 2002;Kurata and Tanji, 1986). Importantly, premotor and primary motor regions have homotopic and heterotopic callosal projections to the contralateral hemisphere (Boussaoud et al, 2005;Fang et al, 2008;Lanz et al, 2017;Marconi et al, 2003). Single neuron recordings in monkeys have shown that anatomically defined subregions of the premotor cortex; the dorsal premotor (PMd) area F2 is particularly involved in the planning and execution of reaching movements and the ventral premotor (PMv) area F5 encodes specific hand actions [for review; (Rizzolatti et al, 2014)].…”