Intelligent behavior demands not only multiple forms of spatial representation, but also coordination among the brain regions mediating those representations. Retrosplenial cortex is densely ...interconnected with the majority of cortical and subcortical brain structures that register an animal's position in multiple internal and external spatial frames of reference. This unique anatomy suggests that it functions to integrate distinct forms of spatial information and provides an interface for transformations between them. Evidence for this was found in rats traversing two different routes placed at different environmental locations. Retrosplenial ensembles robustly encoded conjunctions of progress through the current route, position in the larger environment and the left versus right turning behavior of the animal. Thus, the retrosplenial cortex has the requisite dynamics to serve as an intermediary between brain regions generating different forms of spatial mapping, a result that is consistent with navigational and episodic memory impairments following damage to this region in humans.
Traversal of a complicated route is often facilitated by considering it as a set of related sub-spaces. Such compartmentalization processes could occur within retrosplenial cortex, a structure whose ...neurons simultaneously encode position within routes and other spatial coordinate systems. Here, retrosplenial cortex neurons were recorded as rats traversed a track having recurrent structure at multiple scales. Consistent with a major role in compartmentalization of complex routes, individual retrosplenial cortex (RSC) neurons exhibited periodic activation patterns that repeated across route segments having the same shape. Concurrently, a larger population of RSC neurons exhibited single-cycle periodicity over the full route, effectively defining a framework for encoding of sub-route positions relative to the whole. The same population simultaneously provides a novel metric for distance from each route position to all others. Together, the findings implicate retrosplenial cortex in the extraction of path sub-spaces, the encoding of their spatial relationships to each other, and path integration.
•Retrosplenial cortex encodes sub-routes in complex trajectories•Sub-route encoding manifests as periodic activation at multiple spatial scales•Sub-route encoding cannot be explained purely by movement correlates•Spatially symmetric activation patterns yield a novel metric of distance
Navigation often requires the fragmentation of complex routes into more manageable sub-routes and encoding of their interrelationships. Alexander and Nitz show that retrosplenial cortex represents route sub-spaces via spatially periodic activation patterns. These firing patterns also yield a metric of the animal’s distance from all track locations.
We recorded parietal cortex neurons as rats traversed squared spiral tracks. Spatial firing patterns distinguished the behaviorally identical track segments composing loops, yet recurred with ...increasing or decreasing amplitude across the five loops composing the full track. These results indicate that parietal cortex neurons simultaneously respond to spatial relationships in multiple external reference frames, a phenomenon that may reflect a neural mechanism for relating parts to a whole.
The hippocampal formation (HF) is well documented as having a feedforward, unidirectional circuit organization termed the trisynaptic pathway. This circuit organization exists along the septotemporal ...axis of the HF, but the circuit connectivity across septal to temporal regions is less well described. The emergence of viral genetic mapping techniques enhances our ability to determine the detailed complexity of HF circuitry. In earlier work, we mapped a subiculum (SUB) back projection to CA1 prompted by the discovery of theta wave back propagation from the SUB to CA1 and CA3. We reason that this circuitry may represent multiple extended noncanonical pathways involving the subicular complex and hippocampal subregions CA1 and CA3. In the present study, multiple retrograde viral tracing approaches produced robust mapping results, which supports this prediction. We find significant noncanonical synaptic inputs to dorsal hippocampal CA3 from ventral CA1 (vCA1), perirhinal cortex (Prh), and the subicular complex. Thus, CA1 inputs to CA3 run opposite the trisynaptic pathway and in a temporal to septal direction. Our retrograde viral tracing results are confirmed by anterograde-directed viral mapping of projections from input mapped regions to hippocampal dorsal CA3 (dCA3). We find that genetic inactivation of the projection of vCA1 to dCA3 impairs object-related spatial learning and memory but does not modulate anxiety-related behaviors. Our data provide a circuit foundation to explore novel functional roles contributed by these noncanonical hippocampal circuit connections to hippocampal circuit dynamics and learning and memory behaviors.
Animals in the natural world constantly encounter geometrically complex landscapes. Successful navigation requires that they understand geometric features of these landscapes, including boundaries, ...landmarks, corners and curved areas, all of which collectively define the geometry of the environment
. Crucial to the reconstruction of the geometric layout of natural environments are concave and convex features, such as corners and protrusions. However, the neural substrates that could underlie the perception of concavity and convexity in the environment remain elusive. Here we show that the dorsal subiculum contains neurons that encode corners across environmental geometries in an allocentric reference frame. Using longitudinal calcium imaging in freely behaving mice, we find that corner cells tune their activity to reflect the geometric properties of corners, including corner angles, wall height and the degree of wall intersection. A separate population of subicular neurons encode convex corners of both larger environments and discrete objects. Both corner cells are non-overlapping with the population of subicular neurons that encode environmental boundaries. Furthermore, corner cells that encode concave or convex corners generalize their activity such that they respond, respectively, to concave or convex curvatures within an environment. Together, our findings suggest that the subiculum contains the geometric information needed to reconstruct the shape and layout of naturalistic spatial environments.
The last decade has produced exciting new ideas about retrosplenial cortex (RSC) and its role in integrating diverse inputs. Here, we review the diversity in forms of spatial and directional tuning ...of RSC activity, temporal organization of RSC activity, and features of RSC interconnectivity with other brain structures. We find that RSC anatomy and dynamics are more consistent with roles in multiple sensorimotor and cognitive processes than with any isolated function. However, two more generalized categories of function may best characterize roles for RSC in complex cognitive processes: (1) shifting and relating perspectives for spatial cognition and (2) prediction and error correction for current sensory states with internal representations of the environment. Both functions likely take advantage of RSC’s capacity to encode conjunctions among sensory, motor, and spatial mapping information streams. Together, these functions provide the scaffold for intelligent actions, such as navigation, perspective taking, interaction with others, and error detection.
What is the retrosplenial cortex and what does it do? Alexander et al. discuss theories inspired by these questions and highlight their limitations. They propose that retrosplenial activity serves to relate spatial perspectives and to generate predictions about environmental interactions.
In place of continuous overhead satellite views of an environment, the brain often relies on first-person experiences to estimate spatial relationships between locations. Using new methods, a recent ...study has found the spatial metric observed in hippocampal activity adapts to encode local environmental terrain.
In place of continuous overhead satellite views of an environment, the brain often relies on first-person experiences to estimate spatial relationships between locations. Using new methods, a recent study has found the spatial metric observed in hippocampal activity adapts to encode local environmental terrain.
Flexible navigation demands knowledge of boundaries, routes and their relationships. Within a multi-path environment, a subpopulation of subiculum neurons robustly encoded the axis of travel. The ...firing of axis-tuned neurons peaked bimodally, at head orientations 180° apart. Environmental manipulations showed these neurons to be anchored to environmental boundaries but to lack axis tuning in an open arena. Axis-tuned neurons thus provide a powerful mechanism for mapping relationships between routes and the larger environmental context.
Retrosplenial cortex (RSC) is heavily interconnected with a multitude of cortical regions and is directly connected with the hippocampal formation. As such, it is a likely coordinator of information ...transfer between the hippocampus (HPC) and cortex in the service of spatial cognition and episodic memory. The current work examined three potential temporal frameworks for retrosplenial-hippocampal communication, namely, theta frequency oscillations (6-12 Hz), sharp-wave/ripple events, and repeating, theta phase-locked shifts from low (30-65 Hz) to high (120-160 Hz) gamma frequency oscillations. From simultaneous recordings of single units and local field potentials (LFPs) in RSC and HPC, we report the presence of prominent theta, low-gamma, and high-gamma oscillations in the retrosplenial LFP. Retrosplenial and hippocampal theta rhythms were strongly coherent and subgroups of retrosplenial neurons exhibited either spiking at theta frequencies and/or spike-phase-locking to theta. Retrosplenial neurons were also phase-locked to local low- and high-gamma rhythms, and power in these frequency bands was coupled in a sequential fashion to specific phases of hippocampal and retrosplenial theta rhythms. Coordinated activity between the two regions also occurred during hippocampal sharp-wave/ripple events, where retrosplenial neuron populations were modulated in their spiking and retrosplenial LFPs exhibited sharp-wave-like events that co-occurred with those observed in HPC. These results identify several temporal windows of synchronization between RSC and HPC that may mediate cortico-hippocampal processes related to learning, memory, and spatial representation.
Quick and efficient traversal of learned routes is critical to the survival of many animals. Routes can be defined by both the ordering of navigational epochs, such as continued forward motion or ...execution of a turn, and the distances separating them. The neural substrates conferring the ability to fluidly traverse complex routes are not well understood, but likely entail interactions between frontal, parietal, and rhinal cortices and the hippocampus. This paper demonstrates that posterior parietal cortical neurons map both individual and multiple navigational epochs with respect to their order in a route. In direct contrast to spatial firing patterns of hippocampal neurons, parietal neurons discharged in a place- and direction-independent fashion. Parietal route maps were scalable and versatile in that they were independent of the size and spatial configuration of navigational epochs. The results provide a framework in which to consider parietal function in spatial cognition.
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