Nonspatial Representations Research Articles

Adult-born granule cells facilitate remapping of spatial and non-spatial representations in the dentate gyrus

Adult-born granule cells (abGCs) have been implicated in memory discrimination through a neural computation known as pattern separation. Here, using invivo Ca2+ imaging, we examined how chronic ablation or acute chemogenetic silencing of abGCs affects the activity of mature granule cells (mGCs). In both cases, we observed altered remapping of mGCs. Rather than broadly modulating the activity of all mGCs, abGCs promote the remapping of place cells' firing fields while increasing rate remapping of mGCs that represent sensory cues. In turn, these remapping deficits are associated with behavioral impairments in animals' ability to correctly identify new goal locations. Thus, abGCs facilitate pattern separation through the formation of non-overlapping representations for identical sensory cues encountered in different locations. In the absence of abGCs, the dentate gyrus shifts to a state that is dominated by cue information, a situation that is consistent with the overgeneralization often observed in anxiety or age-related disorders.

Spatialization of Time in the Entorhinal-Hippocampal System.

The functional role of the entorhinal-hippocampal system has been a long withstanding mystery. One key theory that has become most popular is that the entorhinal-hippocampal system represents space to facilitate navigation in one’s surroundings. In this Perspective article, I introduce a novel idea that undermines the inherent uniqueness of spatial information in favor of time driving entorhinal-hippocampal activity. Specifically, by spatializing events that occur in succession (i.e., across time), the entorhinal-hippocampal system is critical for all types of cognitive representations. I back up this argument with empirical evidence that hints at a role for the entorhinal-hippocampal system in non-spatial representation, and computational models of the logarithmic compression of time in the brain.

SpatialRugs: A compact visualization of space and time for analyzing collective movement data

Compact visualization techniques such as dense pixel displays find application in displaying spatio-temporal datasets in a space-efficient way. While mostly focusing on feature development, the depiction of spatial distributions of the movers in these techniques is often traded against better scalability towards the number of moving objects. We propose SpatialRugs, a technique that can be applied to reintroduce spatial positions in such approaches by applying 2D colormaps to determine object locations and which enables users to follow spatio-temporal developments even in non-spatial representations. Geared towards collective movement datasets, we evaluate the applicability of several color maps and discuss limitations. To mitigate perceptional artifacts, we also present and evaluate a custom, time-aware color smoothing method.

Molecular mechanisms within the dentate gyrus and the perirhinal cortex interact during discrimination of similar nonspatial memories.

Differentiating between similar memories is a crucial cognitive function that enables correct episodic memory formation. The ability to separate the components of memories into distinct representations is thought to rely on a computational process known as pattern separation, by which differences are amplified to disambiguate similar events. Although pattern separation has been localized to the dentate gyrus (DG) of the hippocampus and shown to occur in a spatial domain, this cognitive function takes place also during processing of other types of information. In particular, there is some debate on whether the DG participates in pattern separation of nonspatial representations. Considering the classic role of the Prh in the acquisition and storage of object memories in general and tasks with similar features in particular, this cognitive function could rely more heavily on perirhinal regions when object-related information is processed. Here we show that two plasticity-related proteins, BDNF, and Arc, are required in the DG for nonspatial mnemonic differentiation. Moreover, we found that the crucial role of the DG is transient since activity of AMPAR is only required in the Prh but not the DG during differentiated object memory retrieval. Additionally, this memory is not modifiable by postacquisition rhBDNF infusions in the DG that are known to improve memory when given in the Prh. This highlights a differential role of Prh and DG during differentiated object memory consolidation. Additionally, we found that these molecular mechanisms actively interact in the DG and Prh for the formation of distinguishable memories, with infusions of rhBDNF in the Prh being able to rescue mnemonic deficits caused by reduced Arc expression in the DG. These results reveal a complex interaction between plasticity mechanisms in the Prh and DG for nonspatial pattern separation and posit the Prh as the key structure where unique object representations are stored.

Origin and role of path integration in the cognitive representations of the hippocampus: computational insights into open questions.

Path integration is a straightforward concept with varied connotations that are important to different disciplines concerned with navigation, such as ethology, cognitive science, robotics and neuroscience. In studying the hippocampal formation, it is fruitful to think of path integration as a computation that transforms a sense of motion into a sense of location, continuously integrated with landmark perception. Here, we review experimental evidence that path integration is intimately involved in fundamental properties of place cells and other spatial cells that are thought to support a cognitive abstraction of space in this brain system. We discuss hypotheses about the anatomical and computational origin of path integration in the well-characterized circuits of the rodent limbic system. We highlight how computational frameworks for map-building in robotics and cognitive science alike suggest an essential role for path integration in the creation of a new map in unfamiliar territory, and how this very role can help us make sense of differences in neurophysiological data from novel versus familiar and small versus large environments. Similar computational principles could be at work when the hippocampus builds certain non-spatial representations, such as time intervals or trajectories defined in a sensory stimulus space.

Neuronal evidence for good-based economic decisions under variable action costs

Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that “stimulus values” are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space.

Different Brains Process Numbers Differently: Structural Bases of Individual Differences in Spatial and Nonspatial Number Representations

A dominant hypothesis on how the brain processes numerical size proposes a spatial representation of numbers as positions on a "mental number line." An alternative hypothesis considers numbers as elements of a generalized representation of sensorimotor-related magnitude, which is not obligatorily spatial. Here we show that individuals' relative use of spatial and nonspatial representations has a cerebral counterpart in the structural organization of the posterior parietal cortex. Interindividual variability in the linkage between numbers and spatial responses (faster left responses to small numbers and right responses to large numbers; spatial-numerical association of response codes effect) correlated with variations in gray matter volume around the right precuneus. Conversely, differences in the disposition to link numbers to force production (faster soft responses to small numbers and hard responses to large numbers) were related to gray matter volume in the left angular gyrus. This finding suggests that numerical cognition relies on multiple mental representations of analogue magnitude using different neural implementations that are linked to individual traits.

Combinatorial brain decoding of people's whereabouts during visuospatial navigation

Complex behavior typically relies upon many different processes which are related to activity in multiple brain regions. In contrast, neuroimaging analyses typically focus upon isolated processes. Here we present a new approach, combinatorial brain decoding, in which we decode complex behavior by combining the information which we can retrieve from the neural signals about the many different sub-processes. The case in point is visuospatial navigation. We explore the extent to which the route travelled by human subjects (N = 3) in a complex virtual maze can be decoded from activity patterns as measured with functional magnetic resonance imaging. Preliminary analyses suggest that it is difficult to directly decode spatial position from regions known to contain an explicit cognitive map of the environment, such as the hippocampus. Instead, we were able to indirectly derive spatial position from the pattern of activity in visual and motor cortex. The non-spatial representations in these regions reflect processes which are inherent to navigation, such as which stimuli are perceived at which point in time and which motor movement is executed when (e.g., turning left at a crossroad). Highly successful decoding of routes followed through the maze was possible by combining information about multiple aspects of navigation events across time and across multiple cortical regions. This “proof of principle” study highlights how visuospatial navigation is related to the combined activity of multiple brain regions, and establishes combinatorial brain decoding as a means to study complex mental events that involve a dynamic interplay of many cognitive processes.

Perirhinal cortex represents nonspatial, but not spatial, information in rats foraging in the presence of objects: Comparison with lateral entorhinal cortex

The medial temporal lobe (MTL) is involved in mnemonic processing. The perirhinal cortex (PRC) plays a role in object recognition memory, while the hippocampus is required for certain forms of spatial memory and episodic memory. The lateral entorhinal cortex (LEC) receives direct projections from PRC and is one of the two major cortical inputs to the hippocampus. The transformations that occur between PRC and LEC neural representations are not well understood. Here, we show that PRC and LEC had similarly high proportions of neurons with object-related activity (PRC 52/94; LEC 72/153), as expected from their locations in the "what" pathway into the hippocampus. However, LEC unit activity showed more spatial stability than PRC unit activity. A minority of LEC neurons showed stable spatial firing fields away from objects; these firing fields strongly resembled hippocampal place fields. None of the PRC neurons showed this place-like firing. None of the PRC or LEC neurons demonstrated the high firing rates associated with interneurons in hippocampus or medial entorhinal cortex, further dissociating this information processing stream from the path-integration based, movement-related processing of the medial entorhinal cortex and hippocampus. These results provide evidence for nonspatial information processing in the PRC-LEC pathway, as well as showing a functional dissociation between PRC and LEC, with more purely nonspatial representations in PRC and combined spatial-nonspatial representations in LEC.

No inherent left and right side in human ‘mental number line’: evidence from right brain damage

Spatial reasoning has a relevant role in mathematics and helps daily computational activities. It is widely assumed that in cultures with left-to-right reading, numbers are organized along the mental equivalent of a ruler, the mental number line, with small magnitudes located to the left of larger ones. Patients with right brain damage can disregard smaller numbers while mentally setting the midpoint of number intervals. This has been interpreted as a sign of spatial neglect for numbers on the left side of the mental number line and taken as a strong argument for the intrinsic left-to-right organization of the mental number line. Here, we put forward the understanding of this cognitive disability by discovering that patients with right brain damage disregard smaller numbers both when these are mapped on the left side of the mental number line and on the right side of an imagined clock face. This shows that the right hemisphere supports the representation of small numerical magnitudes independently from their mapping on the left or the right side of a spatial-mental layout. In addition, the study of the anatomical correlates through voxel-based lesion-symptom mapping and the mapping of lesion peaks on the diffusion tensor imaging-based reconstruction of white matter pathways showed that the rightward bias in the imagined clock-face was correlated with lesions of high-level middle temporal visual areas that code stimuli in object-centred spatial coordinates, i.e. stimuli that, like a clock face, have an inherent left and right side. In contrast, bias towards higher numbers on the mental number line was linked to white matter damage in the frontal component of the parietal-frontal number network. These anatomical findings show that the human brain does not represent the mental number line as an object with an inherent left and right side. We conclude that the bias towards higher numbers in the mental bisection of number intervals does not depend on left side spatial, imagery or object-centred neglect and that it rather depends on disruption of an abstract non-spatial representation of small numerical magnitudes.

Cross-modal nonspatial repetition inhibition

Although it has been well documented that the spatial inhibitory effect induced by repetition of location (i.e., spatial inhibition of return, or IOR) occurs cross-modally, we do not yet know whether nonspatial (e.g., color-based) repetition-induced inhibition occurs in a cross-modal fashion as well. In the present study, a novel cross-modal paradigm with regard to color-based repetition was adopted. An intervening neutral cue, whose semantic identity was different from those of both the prime and the target, was introduced between the prime and the target in a repetition-priming task. The modalities of the prime, the neutral cue, and the target could be either visual or auditory, and the prime and the target could refer either to the same or to different semantic identities. By adopting this paradigm, we aimed to answer two questions: (1) What are the specific conditions under which cross-modal semantic-based repetition inhibition occurs? (2) Are the representations inhibited in the semantic-based repetition inhibition effect supramodal or modality-specific? Our results suggested that semantic-based repetition inhibition occurs only when the prime and the neutral cue are from the same sensory modality, and it occurs irrespective of whether the modality of the target is cued and irrespective of whether the modality of the target is auditory or visual. Taken together, our results suggest that the occurrence of cross-modal nonspatial repetition inhibition is conditional and that the nonspatial representations inhibited by the repetition inhibition are supramodal.

Distinct or Gradually Changing Spatial and Nonspatial Representations along the Dorsoventral Axis of the Hippocampus

The hippocampus provides neuroscientists with one of the most striking neural phenomena in any high-order brain area: the encoding of the animal's self location. As the animal moves through the environment, individual hippocampal pyramidal cells become active, mainly when the animal passes through a

The posterior parietal cortex and non-spatial cognition

The primate posterior parietal cortex (PPC) processes information related to environmental physical space. The human PPC has apparently expanded not only in size but also in its functional range to encompass certain abstract and higher-order conceptual spaces. In this report, we review various forms of non-spatial representation in the PPC. These forms are presented roughly in order of the level of abstraction of the ‘objects’ and pseudo-spatial relations represented. Also, we consider mechanisms that could have enabled the hominid PPC to establish such representations. Lastly, we offer a general principle to unify the newer forms of representation with the original functions of the PPC.

Attention Enhances the Retrieval and Stability of Visuospatial and Olfactory Representations in the Dorsal Hippocampus

Author SummaryAttention modulates the encoding and retrieval of memories, but the physiological basis of this interaction has largely been unexplored. The formation of memories which depend on the hippocampus involves the conscious recall of events that occur in specific spatial contexts, a form of memory known as episodic. To investigate the physiological consequences of the interaction between attention and memory in the hippocampus, we recorded single-cell activity and local field potentials — the local rhythmic oscillatory activity of neurons — from the same cells over several days while animals learned one of two goal-oriented tasks. In the visuospatial version of the task, mice had to associate a specific spatial location with a reward, independent of an odor cue. In the nonspatial, olfactory version, mice had to associate a specific odor with the food reward, independent of spatial location. We found that, during periods of navigation, only neurons in the visuospatially trained animals displayed long-term stable representations of space, and neuronal synchronization to so-called gamma oscillations, a mechanism of signal amplification that has been proposed to underlie attentional processes. Conversely, when animals were sniffing the odors in fixed spatial locations, only neurons in the olfactory-trained group displayed a stable increase in firing rate in response to the reward-associated odor. Our data suggest that attention modulates what is encoded and retrieved by hippocampal cells and that neuronal synchronization to gamma oscillations may underlie the mechanism whereby attention leads to stable spatial memory retrieval during navigation.

An outline of the primal sketch in human vision

The primal sketch is a symbolic, two-dimensional description of the significant grey-level changes in an image. Psychophysical evidence suggests a primal sketch in human vision, rather like that proposed by Marr, although different in many details. The most important differences are that the human version does not have an address-based geometrical representation of space, and that the process of spatial representation may be by-passed for certain dense contour arrangements. The primal sketch in human vision is not automatic: there is a control structure that selects the spatial scale over which spatial representation occurs. By using a range of spatial filters, the visual system identifies and locates the basic features (lines, edges, corners and intersections). The mechanisms whereby the visual system combines the information from the different filters is designed to make the extreme spatial scales explicit and uses the largest scale to group the finer scales, creating a two level hierarchy in which the spatial relations between different groups of features are represented in a quasi-Euclidean geometry, but the elements within a group are only accorded an impoverished, perhaps non-spatial representation.