scholarly journals Visual cues determine hippocampal directional selectivity

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.

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.


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)


1998 ◽  
Vol 80 (1) ◽  
pp. 425-446 ◽  
Author(s):  
James J. Knierim ◽  
Hemant S. Kudrimoti ◽  
Bruce L. McNaughton

Knierim, James J., Hemant S. Kudrimoti, and Bruce L. McNaughton. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80: 425–446, 1998. Two types of neurons in the rat brain have been proposed to participate in spatial learning and navigation: place cells, which fire selectively in specific locations of an environment and which may constitute key elements of cognitive maps, and head direction cells, which fire selectively when the rat's head is pointed in a specific direction and which may serve as an internal compass to orient the cognitive map. The spatially and directionally selective properties of these cells arise from a complex interaction between input from external landmarks and from idiothetic cues; however, the exact nature of this interaction is poorly understood. To address this issue, directional information from visual landmarks was placed in direct conflict with directional information from idiothetic cues. When the mismatch between the two sources of information was small (45°), the visual landmarks had robust control over the firing properties of place cells; when the mismatch was larger, however, the firing fields of the place cells were altered radically, and the hippocampus formed a new representation of the environment. Similarly, the visual cues had control over the firing properties of head direction cells when the mismatch was small (45°), but the idiothetic input usually predominated over the visual landmarks when the mismatch was larger. Under some conditions, when the visual landmarks predominated after a large mismatch, there was always a delay before the visual cues exerted their control over head direction cells. These results support recent models proposing that prewired intrinsic connections enable idiothetic cues to serve as the primary drive on place cells and head direction cells, whereas modifiable extrinsic connections mediate a learned, secondary influence of visual landmarks.


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.


2014 ◽  
Vol 281 (1787) ◽  
pp. 20140634 ◽  
Author(s):  
Matthew Collett

Insects such as desert ants learn stereotyped visual routes between their nests and reliable food sites. Studies here reveal an important control element for ensuring that the route memories are used appropriately. They find that visual route memories can be disengaged, so that they do not provide guidance, even when all appropriate visual cues are present and when there are no competing guidance cues. Ants were trained along a simple route dominated by a single isolated landmark. If returning ants were caught just before entering the nest and replaced at the feeder, then they often interrupted the recapitulation of their homeward route with a period of apparent confusion during which the route memories were ignored. A series of experiments showed that this confusion occurred in response to the repetition of the route, and that the ants must therefore maintain some kind of a memory of their visual experience on the current trip home. A conceptual model of route guidance is offered to explain the results here. It proposes how the memory might act and suggests a general role for disengagement in regulating route guidance.


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.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Romain Bourboulou ◽  
Geoffrey Marti ◽  
François-Xavier Michon ◽  
Elissa El Feghaly ◽  
Morgane Nouguier ◽  
...  

The ability to flexibly navigate an environment relies on a hippocampal-dependent cognitive map. External space can be internally mapped at different spatial resolutions. However, whether hippocampal spatial coding resolution can rapidly adapt to local features of an environment remains unclear. To explore this possibility, we recorded the firing of hippocampal neurons in mice navigating virtual reality environments, embedding or not local visual cues (virtual 3D objects) in specific locations. Virtual objects enhanced spatial coding resolution in their vicinity with a higher proportion of place cells, smaller place fields, increased spatial selectivity and stability. This effect was highly dynamic upon objects manipulations. Objects also improved temporal coding resolution through improved theta phase precession and theta timescale spike coordination. We propose that the fast adaptation of hippocampal spatial coding resolution to local features of an environment could be relevant for large-scale navigation.


1995 ◽  
Vol 198 (10) ◽  
pp. 2049-2054 ◽  
Author(s):  
G Nevitt ◽  
N Pentcheff ◽  
K Lohmann ◽  
R Zimmer-Faust

Western Atlantic spiny lobsters (Panulirus argus) are superb underwater navigators. Spiny lobsters perform dramatic seasonal offshore migrations and have also been shown to locate and home to specific den sites within the elaborate coral reef environment in which they live. How these animals perform such complex orientation tasks is not known. The study reported here was designed to explore the sensory mechanisms that spiny lobsters use to orient in and around a familiar patch reef environment. Our results show that, in the absence of visual cues, lobsters displaced a short (50 m) distance off the reef do not initially (i.e. within 20 min) travel towards their dens or return to the patch reef where their dens are located. Instead, the headings lobsters follow are significantly correlated to the direction of local hydrodynamic cues and, specifically, to the direction of approaching wave surge. Results from ultrasonic tracking experiments over longer periods (24 h) suggest that displaced lobsters are able to relocate the reef where they were captured, even without visual cues. These results suggest that hydrodynamic cues may provide useful and immediate directional information to lobsters within the local environment of the home reef.


Author(s):  
Belinda J Liddell ◽  
Gin S Malhi ◽  
Kim L Felmingham ◽  
Miriam Den ◽  
Pritha Das ◽  
...  

Abstract Social attachment systems are disrupted for refugees through trauma and forced displacement. This study tested how the attachment system mitigates neural responses to threat in refugees with PTSD. Refugees with PTSD (N=28) and refugee trauma-exposed controls (N=22) viewed threat-related stimuli primed by attachment cues during fMRI. We examined group differences and the moderating effects of avoidant or anxious attachment style, and grief related to separation from family, on brain activity and connectivity patterns. Separation grief was associated with increased amygdala but decreased ventromedial prefrontal (VMPFC) cortical activity to the attachment prime, and decreased VMPFC and hippocampal activity to attachment primed threat in the PTSD (vs TEC) group. Avoidant attachment style was connected with increased dorsal frontoparietal attention regional activity to attachment prime cues in the PTSD group. Anxious attachment style was associated with reduced left amygdala connectivity with left medial prefrontal regions to attachment primed threat in the PTSD group. Separation grief appears to reduce attachment buffering of threat reactivity in refugees with PTSD, while avoidant and anxious attachment style modulated attentional and prefrontal regulatory mechanisms in PTSD respectively. Considering social attachments in refugees could be important to post-trauma recovery, based within changes in key emotion regulation brain systems.


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