scholarly journals Hippocampal representations of distance, space, and direction and their plasticity predict navigational performance

2021 ◽  
Author(s):  
Jason J Moore ◽  
Jesse D Cushman ◽  
Lavanya Acharya ◽  
Mayank R Mehta

ABSTRACTThe hippocampus is implicated in episodic memory and allocentric spatial navigation. However, spatial selectivity is insufficient to navigate; one needs information about the distance and direction to the reward on a specific journey. The nature of these representations, whether they are expressed in an episodic-like sequence, and their relationship with navigational performance are unknown. We recorded single units from dorsal CA1 of the hippocampus while rats navigated to an unmarked reward zone defined solely by distal visual cues, similar to the classic water maze. The allocentric spatial selectivity was substantially weaker than in typical real world tasks, despite excellent navigational performance. Instead, the majority of cells encoded path distance from the start of trials. Cells also encoded the rat’s allocentric position and head angle. Often the same cells multiplexed and encoded path distance, head direction and allocentric position in a sequence, thus encoding a journey-specific episode. The strength of neural activity and tuning strongly correlated with performance, with a temporal relationship indicating neural responses influencing behavior and vice versa. Consistent with computational models of associative Hebbian learning, neural responses showed increasing clustering and became better predictors of behaviorally relevant variables, with neurometric curves exceeding and converging to psychometric curves. These findings demonstrate that hippocampal neurons multiplex and exhibit highly plastic, task- and experience-dependent tuning to path-centric and allocentric variables to form an episode, which could mediate navigation.

2015 ◽  
Author(s):  
Lavanya Acharya ◽  
Zahra M. Aghajan ◽  
Cliff Vuong ◽  
Jason Moore ◽  
Mayank Mehta

Both spatial and directional information are necessary for navigation. Rodent hippocampal neurons show spatial selectivity in all environments, but directional tuning only on linear paths. The sensory mechanisms underlying directionality are unknown, though vestibular and visual cues are thought to be crucial. However, hippocampal neurons are thought to show no angular modulation during two-dimensional random foraging despite the presence of vestibular and visual cues. Additionally, specific aspects of visual cues have not been directly linked to hippocampal responses in rodents. To resolve these issues we manipulated vestibular and visual cues in a series of experiments. We first measured hippocampal activity during random foraging in real world (RW) where we found that neurons’ firing exhibited significant modulation by head-direction. In fact, the fraction of modulated neurons was comparable to that in the head-direction system. These findings are contrary to commonly held beliefs about hippocampal directionality. To isolate the contribution of visual cues we measured neural responses in a visually similar virtual reality (VR) where the range of vestibular inputs is minimized. Significant directional modulation was not only found in VR, but it was comparable to that in RW. Several additional experiments revealed that changes in the angular information contained in the visual cues induced corresponding changes in hippocampal head-directional modulation. Remarkably, for head-directionally modulated neurons, the ensemble activity was biased towards the sole visual cue. These results demonstrate that robust vestibular cues are not required for hippocampal directional selectivity, while visual cues are not only sufficient but also play a causal role in driving hippocampal responses.


1993 ◽  
Vol 70 (4) ◽  
pp. 1516-1529 ◽  
Author(s):  
T. Ono ◽  
K. Nakamura ◽  
H. Nishijo ◽  
S. Eifuku

1. Neural activity in the monkey hippocampal formation (HF) was analyzed during a spatial moving task in which the monkey was guided by auditory and visual cues and when stimuli were presented from various directions. The monkey could control a motorized, movable device (cab) and its route to a target location by pressing the proper one of five available bars in an appropriate sequence (spatial moving task). In any of several locations in the field, neural responses were evident in relation to the presentation of various objects or human movement in some relative direction (left, anterior, right) as a directional stimulus test. 2. Of 238 hippocampal neurons analyzed, 172 (72.3%, 238-66) responded in either the spatial moving task, or to the direction from which stimulation was presented, or to the location of the monkey in the field, or to some combination of these. 3. The activity of 79 (33.2%) neurons was higher when the monkey was in some specific location in the field during the spatial moving task, regardless of the approach route or other task parameters (place related neurons). 4. Responses to the task cues in the spatial moving task were evident in 110 (46.3%) neurons (task related neurons). Of these, 77 (32.4%) neurons were not place related. The remaining 33 (13.9%) neurons were both task related and place related. These neurons responded to task cues in only that part of the field in which place related responses occurred. The neural response to the task cues disappeared when the monkey moved out of the place response region. The place related and task related neural responses disappeared when the room light was switched off. Thus information from the environment outside of the cab contributed to the place related and task related responses. 5. Stimuli presented from certain specific directions induced responses, selectively, in 41 (17.2%) of the neurons (direction related neurons). The dependence of the preferred direction was described in one of three ways--egocentric, allocentric, or place-direction specific. Nineteen egocentric neurons responded to a stimulus only when it was presented from a certain direction relative to the orientation of the monkey, regardless of the location of the monkey. Eleven allocentric neurons responded to a stimulus only when it was presented at a particular position in the room, regardless of the location or orientation of the monkey.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
Vol 118 (45) ◽  
pp. e2105646118
Author(s):  
Martin Schrimpf ◽  
Idan Asher Blank ◽  
Greta Tuckute ◽  
Carina Kauf ◽  
Eghbal A. Hosseini ◽  
...  

The neuroscience of perception has recently been revolutionized with an integrative modeling approach in which computation, brain function, and behavior are linked across many datasets and many computational models. By revealing trends across models, this approach yields novel insights into cognitive and neural mechanisms in the target domain. We here present a systematic study taking this approach to higher-level cognition: human language processing, our species’ signature cognitive skill. We find that the most powerful “transformer” models predict nearly 100% of explainable variance in neural responses to sentences and generalize across different datasets and imaging modalities (functional MRI and electrocorticography). Models’ neural fits (“brain score”) and fits to behavioral responses are both strongly correlated with model accuracy on the next-word prediction task (but not other language tasks). Model architecture appears to substantially contribute to neural fit. These results provide computationally explicit evidence that predictive processing fundamentally shapes the language comprehension mechanisms in the human brain.


2013 ◽  
Author(s):  
Zahra Aghajan ◽  
Lavanya Acharya ◽  
Jesse Cushman ◽  
Cliff Vuong ◽  
Jason Moore ◽  
...  

Dorsal Hippocampal neurons provide an allocentric map of space, characterized by three key properties. First, their firing is spatially selective, termed a rate code. Second, as animals traverse through place fields, neurons sustain elevated firing rates for long periods, however this has received little attention. Third the theta-phase of spikes within this sustained activity varies with animal's location, termed phase-precession or a temporal code. The precise relationship between these properties and the mechanisms governing them are not understood, although distal visual cues (DVC) are thought to be sufficient to reliably elicit them. Hence, we measured rat CA1 neurons' activity during random foraging in two-dimensional VR—where only DVC provide consistent allocentric location information— and compared it with their activity in real world (RW). Surprisingly, we found little spatial selectivity in VR. This is in sharp contrast to robust spatial selectivity commonly seen in one-dimensional RW and VR, or two-dimensional RW. Despite this, neurons in VR generated approximately two-second long phase precessing spike sequences, termed “hippocampal motifs”. Motifs, and “Motif-fields”, an aggregation of all motifs of a neuron, had qualitatively similar properties including theta-scale temporal coding in RW and VR, but the motifs were far less spatially localized in VR. These results suggest that intrinsic, network mechanisms generate temporally coded hippocampal motifs, which can be dissociated from their spatial selectivity. Further, DVC alone are insufficient to localize motifs spatially to generate a robust rate code.


2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.


2001 ◽  
Vol 86 (2) ◽  
pp. 692-702 ◽  
Author(s):  
Michaël B. Zugaro ◽  
Eiichi Tabuchi ◽  
Céline Fouquier ◽  
Alain Berthoz ◽  
Sidney I. Wiener

Head direction (HD) cells discharge selectively in macaques, rats, and mice when they orient their head in a specific (“preferred”) direction. Preferred directions are influenced by visual cues as well as idiothetic self-motion cues derived from vestibular, proprioceptive, motor efferent copy, and command signals. To distinguish the relative importance of active locomotor signals, we compared HD cell response properties in 49 anterodorsal thalamic HD cells of six male Long-Evans rats during active displacements in a foraging task as well as during passive rotations. Since thalamic HD cells typically stop firing if the animals are tightly restrained, the rats were trained to remain immobile while drinking water distributed at intervals from a small reservoir at the center of a rotatable platform. The platform was rotated in a clockwise/counterclockwise oscillation to record directional responses in the stationary animals while the surrounding environmental cues remained stable. The peak rate of directional firing decreased by 27% on average during passive rotations ( r 2 = 0.73, P< 0.001). Individual cells recorded in sequential sessions ( n = 8) reliably showed comparable reductions in peak firing, but simultaneously recorded cells did not necessarily produce identical responses. All of the HD cells maintained the same preferred directions during passive rotations. These results are consistent with the hypothesis that the level of locomotor activity provides a state-dependent modulation of the response magnitude of AD HD cells. This could result from diffusely projecting neuromodulatory systems associated with motor state.


Author(s):  
Cheng Lyu ◽  
L.F. Abbott ◽  
Gaby Maimon

AbstractMany behavioral tasks require the manipulation of mathematical vectors, but, outside of computational models1–8, it is not known how brains perform vector operations. Here we show how the Drosophila central complex, a region implicated in goal-directed navigation8–14, performs vector arithmetic. First, we describe neural signals in the fan-shaped body that explicitly track a fly’s allocentric traveling direction, that is, the traveling direction in reference to external cues. Past work has identified neurons in Drosophila12,15–17 and mammals18,19 that track allocentric heading (e.g., head-direction cells), but these new signals illuminate how the sense of space is properly updated when traveling and heading angles differ. We then characterize a neuronal circuit that rotates, scales, and adds four vectors related to the fly’s egocentric traveling direction–– the traveling angle referenced to the body axis––to compute the allocentric traveling direction. Each two-dimensional vector is explicitly represented by a sinusoidal activity pattern across a distinct neuronal population, with the sinusoid’s amplitude representing the vector’s length and its phase representing the vector’s angle. The principles of this circuit, which performs an egocentric-to-allocentric coordinate transformation, may generalize to other brains and to domains beyond navigation where vector operations or reference-frame transformations are required.


2020 ◽  
Author(s):  
Johannes Schultz ◽  
Chris D. Frith

To survive, all animals need to predict what other agents are going to do next. The first step is to detect that an object is an agent and, if so, how sophisticated it is. To this end, visual cues are especially important: the form of the agent and the nature of its movements. Once identified, the movements of an agent, however sophisticated, can be anticipated in the short term on the basis of purely physical constraints, but, in the longer term, it is useful to take account of the agent’s goals and intentions. Goal directed agents are marked by the rationality of their movements, reaching their goals by the shortest or least effortful path. Observing goal directed behaviour activates the brain’s action observation/mirror neuron network. The observer’s own action generating mechanism has an important role in predicting future movements of goal directed agents.Intentions have a critical role in determining actions when agents interact with other agents. In such interactions, movements can become communicative rather than directed to immediate goals. Also, each agent can be trying to predict the behaviour of the other, leading to a recursive arms race. It is difficult to infer intentional behaviour from movement kinematics and interpretation is much more dependent upon prior beliefs about the agent. When people believe that they are interacting with an intentional agent, the brain’s mentalising system is activated as the person tries to assess the degree of sophistication of the agent. Several biologically-constrained computational models of action recognition are available, but equivalent models for understanding intentional agents remain to be developed.


2017 ◽  
Vol 29 (2) ◽  
pp. 202-211
Author(s):  
Ryoko Furukawa ◽  
Martha Driessnack ◽  
Eiko Kobori

Japanese communication relies heavily on nonverbal cues and context. The purpose of this study was to examine the impact of video-mediated communication (VMC) on communication satisfaction and marital relationships in young couples separated during the perinatal period as they honor the Japanese tradition of Satogaeri Bunben. Couples were assigned to the VMC treatment group ( n = 14) or control group ( n = 13). A mixed-methods approach to data collection and analysis was used. Longitudinal quantitative analysis from the Primary Communication Inventory and Intimate Bond Measure revealed significant differences between the Husband groups. Primary Communication Inventory and Intimate Bond Measure were strongly correlated regardless of group. Qualitative analysis of participant diaries revealed the addition of visual cues helped create a sense of “virtual co-presence,” which was both positive and negative. In conclusion, VMC appears to improve communication in the separated Japanese perinatal couples, especially through the addition of visual cues provided with VMC.


2011 ◽  
Vol 105 (6) ◽  
pp. 2989-3001 ◽  
Author(s):  
Ryan M. Yoder ◽  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Mignon V. Lamia ◽  
Stephane Valerio ◽  
...  

Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.


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