Visuomotor interactions in the mouse forebrain mediated by extrastriate cortico-cortical pathways.

Introduction: The mammalian visual system can be broadly divided into two functional processing pathways: a dorsal stream supporting visually and spatially guided actions, and a ventral stream enabling object recognition. In rodents, the majority of visual signaling in the dorsal stream is transmitted to frontal motor cortices via extrastriate visual areas surrounding V1, but exactly where and to what extent V1 feeds into motor-projecting visual regions is not well known. Methods: We employed a dual labeling strategy in male and female mice in which efferent projections from V1 were labeled anterogradely, and motor-projecting neurons in higher visual areas were labeled with retrogradely traveling adeno-associated virus (rAAV-retro) injected in M2. We characterized the labeling in both flattened and coronal sections of dorsal cortex and made high-resolution 3D reconstructions to count putative synaptic contacts in different extrastriate areas. Results: The most pronounced colocalization V1 output and M2 input occurred in extrastriate areas AM, PM, RL and AL. Neurons in both superficial and deep layers in each project to M2, but high resolution volumetric reconstructions indicated that the majority of putative synaptic contacts from V1 onto M2-projecting neurons occurred in layer 2/3. Discussion: These findings support the existence of a dorsal processing stream in the mouse visual system, where visual signals reach motor cortex largely via feedforward projections in anteriorly and medially located extrastriate areas.

Action representation in the mouse parieto-frontal network.

The posterior parietal cortex (PPC) and frontal motor areas comprise a cortical network supporting goal-directed behaviour, with functions including sensorimotor transformations and decision making. In primates, this network links performed and observed actions via mirror neurons, which fire both when individuals perform an action and when they observe the same action performed by a conspecific. Mirror neurons are believed to be important for social learning, but it is not known whether mirror-like neurons occur in similar networks in other social species, such as rodents, or if they can be measured in such models using paradigms where observers passively view a demonstrator. Therefore, we imaged Ca2+ responses in PPC and secondary motor cortex (M2) while mice performed and observed pellet-reaching and wheel-running tasks, and found that cell populations in both areas robustly encoded several naturalistic behaviours. However, neural responses to the same set of observed actions were absent, although we verified that observer mice were attentive to performers and that PPC neurons responded reliably to visual cues. Statistical modelling also indicated that executed actions outperformed observed actions in predicting neural responses. These results raise the possibility that sensorimotor action recognition in rodents could take place outside of the parieto-frontal circuit, and underscore that detecting socially-driven neural coding depends critically on the species and behavioural paradigm used.

Organization of Posterior Parietal-Frontal Connections in the Rat.

Recent investigations of the rat posterior parietal cortex (PPC) suggest that this region plays a central role in action control together with the frontal cortical areas. Posterior parietal-frontal cortical connections have been described in rats, but little is known about whether these connections are topographically organized as in the primate. Here, we injected retrograde and anterograde tracers into subdivisions of PPC as well as the frontal midline and orbital cortical areas to explore possible topographies within their connections. We found that PPC projects to several frontal cortical areas, largely reciprocating the densest input received from the same areas. All PPC subdivisions are strongly connected with the secondary motor cortex (M2) in a topographically organized manner. The medial subdivision (medial posterior parietal cortex, mPPC) has a dense reciprocal connection with the most caudal portion of M2 (cM2), whereas the lateral subdivision (lateral posterior parietal cortex, lPPC) and the caudolateral subdivision (PtP) are reciprocally connected with the intermediate rostrocaudal portion of M2 (iM2). Sparser reciprocal connections were seen with anterior cingulate area 24b. mPPC connects with rostral, and lPPC and PtP connect with caudal parts of 24b, respectively. There are virtually no connections with area 24a, nor with prelimbic or infralimbic cortex. PPC and orbitofrontal cortices are also connected, showing a gradient such that mPPC entertains reciprocal connections mainly with the ventral orbitofrontal cortex (OFC), whereas lPPC and PtP are preferentially connected with medial and central portions of ventrolateral OFC, respectively. Our results thus indicate that the connections of PPC with frontal cortices are organized in a topographical fashion, supporting functional heterogeneity within PPC and frontal cortices.

Architecture and organization of mouse posterior parietal cortex relative to extrastriate areas.

The posterior parietal cortex (PPC) is a multifaceted region of cortex, contributing to several cognitive processes, including sensorimotor integration and spatial navigation. Although recent years have seen a considerable rise in the use of rodents, particularly mice, to investigate PPC and related networks, a coherent anatomical definition of PPC in the mouse is still lacking. To address this, we delineated the mouse PPC, using cyto- and chemoarchitectural markers from Nissl-, parvalbumin-and muscarinic acetylcholine receptor M2-staining. Additionally, we performed bilateral triple anterograde tracer injections in primary visual cortex (V1) and prepared flattened tangential sections from one hemisphere and coronal sections from the other, allowing us to co-register the cytoarchitectural features of PPC with V1 projections. This revealed that extrastriate area A was largely contained within lateral PPC, that medial PPC overlapped with the anterior portion of area AM, and that anterior RL overlapped partially with area PtP. Furthermore, triple anterograde tracer injections in PPC showed strong projections to associative thalamic nuclei as well as higher visual areas, orbitofrontal, cingulate and secondary motor cortices. Retrograde circuit mapping with rabies virus further showed that all cortical connections were reciprocal. These combined approaches provide a coherent definition of mouse PPC that incorporates laminar architecture, extrastriate projections, thalamic, and cortico-cortical connections.