scholarly journals Transformation of the head-direction signal into a spatial code

2016 ◽  
Author(s):  
Adrien Peyrache ◽  
Natalie Schieferstein ◽  
Gyorgy Buzsaki

AbstractAnimals integrate multiple sensory inputs to successfully navigate in their environments. Head direction (HD), boundary vector, grid and place cells in the entorhinal-hippocampal system form the brain’s navigational system that allows to identify the animal’s current location, but how the functions of these specialized neuron types are acquired remain to be understood. Here we report that activity of HD neurons are influenced by the ambulatory constraints imposed upon the animal by the boundaries of the explored environment, leading to spurious spatial information. However, in the post-subiculum, the main cortical stage of HD signal processing, HD neurons convey true spatial information in the form of border modulated activity through the integration of additional sensory modalities relative to egocentric position, unlike their driving thalamic inputs. These findings demonstrate how the combination of HD and egocentric information can be transduced into a spatial code.


2018 ◽  
Author(s):  
Xiaoyang Long ◽  
Sheng-Jia Zhang

AbstractSpatially selective firing in the forms of place cells, grid cells, boundary vector/border cells and head direction cells are the basic building blocks of a canonical spatial navigation system centered on the hippocampal-entorhinal complex. While head direction cells can be found throughout the brain, spatial tuning outside the hippocampal formation are often non-specific or conjunctive to other representations such as a reward. Although the precise mechanism of spatially selective activities is not understood, various studies show sensory inputs (particularly vision) heavily modulate spatial representation in the hippocampal-entorhinal circuit. To better understand the contribution from other sensory inputs in shaping spatial representation in the brain, we recorded from the primary somatosensory cortex in foraging rats. To our surprise, we were able to identify the full complement of spatial activity patterns reported in the hippocampal-entorhinal network, namely, place cells, head direction cells, boundary vector/border cells, grid cells and conjunctive cells. These newly identified somatosensory spatial cell types form a spatial map outside the hippocampal formation and support the hypothesis that location information is necessary for body representation in the somatosensory cortex, and may be analogous to spatially tuned representations in the motor cortex relating to the movement of body parts. Our findings are transformative in our understanding of how spatial information is used and utilized in the brain, as well as functional operations of the somatosensory cortex in the context of rehabilitation with brain-machine interfaces.



Author(s):  
Xiaoyang Long ◽  
Sheng-Jia Zhang

AbstractSpatially selective firing of place cells, grid cells, boundary vector/border cells and head direction cells constitutes the basic building blocks of a canonical spatial navigation system centered on the hippocampal-entorhinal complex. While head direction cells can be found throughout the brain, spatial tuning outside the hippocampal formation is often non-specific or conjunctive to other representations such as a reward. Although the precise mechanism of spatially selective firing activity is not understood, various studies show sensory inputs, particularly vision, heavily modulate spatial representation in the hippocampal-entorhinal circuit. To better understand the contribution of other sensory inputs in shaping spatial representation in the brain, we performed recording from the primary somatosensory cortex in foraging rats. To our surprise, we were able to detect the full complement of spatially selective firing patterns similar to that reported in the hippocampal-entorhinal network, namely, place cells, head direction cells, boundary vector/border cells, grid cells and conjunctive cells, in the somatosensory cortex. These newly identified somatosensory spatial cells form a spatial map outside the hippocampal formation and support the hypothesis that location information modulates body representation in the somatosensory cortex. Our findings provide transformative insights into our understanding of how spatial information is processed and integrated in the brain, as well as functional operations of the somatosensory cortex in the context of rehabilitation with brain-machine interfaces.



2019 ◽  
Author(s):  
Felicia Pei-Hsin Cheng ◽  
Adem Saglam ◽  
Selina André ◽  
Arezoo Pooresmaeili

AbstractReward value guides goal-directed behavior and modulates early sensory processing. Rewarding stimuli are often multisensory but it is not known how reward value is combined across sensory modalities. Here we show that the integration of reward value critically depends on whether the distinct sensory inputs are perceived to emanate from the same multisensory object. We systematically manipulated the congruency in monetary reward values and the relative spatial positions of co-occurring auditory and visual stimuli that served as bimodal distractors during an oculomotor task. The amount of interference induced by the distractors was used as an indicator of their perceptual salience. Our results across two experiments show that when reward value is linked to each modality separately, the value congruence between vision and audition determines the combined salience of the bimodal distractors. However, reward value of vision wins over the value of audition if visual and auditory stimuli have been experienced as belonging to the same audiovisual object prior to the learning of the reward values. The perceived spatial alignment of auditory and visual stimuli is a prerequisite for the integration of their reward values, as no effect of reward value was observed when the two modalities were perceived to be misaligned. These results show that in a task that highly relies on the processing of visual spatial information, the reward values from multiple sensory modalities are integrated with each other, each with their respective weights. This weighting depends on the congruency in reward values, exposure history, and spatial co-localization.



2015 ◽  
pp. 77-85
Author(s):  
Peter J. Zeno

A unique roving robot navigational system is presented here, which is inspired by rats’ navigational and spatial awareness brain cells. Rodents, as well as all mammalians, are capable of exploring their surroundings when foraging or avoiding predators, and remembering their way home or to the closest known shelter through path integration. This is true for other creatures, but the neural cells involved in accomplishing these tasks have been most notably studied in rats, as they share certain similarities with a human’s brain. The robot built in this study, named ratbot, uses characteristics and interpreted functionalities of the specialized navigational and spatial cognition brain cells, which are primarily found in the hippocampus and entorhinal cortex. These cells are the: place cells, head direction cells, boundary cells, and grid cells, as well as memory used for the storage and access of salient distal cues. Similar to a rat, the ratbot uses path integration to navigate from one waypoint to another. This is accomplished through use of vectors and vector mathematics. Additionally, the ratbot uses a field programmable gate array (FPGA) to emulate grid cell inspired functionality for environment mapping and spatial cognition.



2021 ◽  
pp. 1-12
Author(s):  
Georg F. Striedter ◽  
R. Glenn Northcutt

Comparative neurobiologists have long wondered when and how the dorsal pallium (e.g., mammalian neocortex) evolved. For the last 50 years, the most widely accepted answer has been that this structure was already present in the earliest vertebrates and, therefore, homologous between the major vertebrate lineages. One challenge for this hypothesis is that the olfactory bulbs project throughout most of the pallium in the most basal vertebrate lineages (notably lampreys, hagfishes, and lungfishes) but do not project to the putative dorsal pallia in teleosts, cartilaginous fishes, and amniotes (i.e., reptiles, birds, and mammals). To make sense of these data, one may hypothesize that a dorsal pallium existed in the earliest vertebrates and received extensive olfactory input, which was subsequently lost in several lineages. However, the dorsal pallium is notoriously difficult to delineate in many vertebrates, and its homology between the various lineages is often based on little more than its topology. Therefore, we suspect that dorsal pallia evolved independently in teleosts, cartilaginous fishes, and amniotes. We further hypothesize that the emergence of these dorsal pallia was accompanied by the phylogenetic restriction of olfactory projections to the pallium and the expansion of inputs from other sensory modalities. We do not deny that the earliest vertebrates may have possessed nonolfactory sensory inputs to some parts of the pallium, but such projections alone do not define a dorsal pallium.



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.



2009 ◽  
Vol 21 (12) ◽  
pp. 2384-2397 ◽  
Author(s):  
Valerio Santangelo ◽  
Marta Olivetti Belardinelli ◽  
Charles Spence ◽  
Emiliano Macaluso

In everyday life, the allocation of spatial attention typically entails the interplay between voluntary (endogenous) and stimulus-driven (exogenous) attention. Furthermore, stimuli in different sensory modalities can jointly influence the direction of spatial attention, due to the existence of cross-sensory links in attentional control. Using fMRI, we examined the physiological basis of these interactions. We induced exogenous shifts of auditory spatial attention while participants engaged in an endogenous visuospatial cueing task. Participants discriminated visual targets in the left or right hemifield. A central visual cue preceded the visual targets, predicting the target location on 75% of the trials (endogenous visual attention). In the interval between the endogenous cue and the visual target, task-irrelevant nonpredictive auditory stimuli were briefly presented either in the left or right hemifield (exogenous auditory attention). Consistent with previous unisensory visual studies, activation of the ventral fronto-parietal attentional network was observed when the visual targets were presented at the uncued side (endogenous invalid trials, requiring visuospatial reorienting), as compared with validly cued targets. Critically, we found that the side of the task-irrelevant auditory stimulus modulated these activations, reducing spatial reorienting effects when the auditory stimulus was presented on the same side as the upcoming (invalid) visual target. These results demonstrate that multisensory mechanisms of attentional control can integrate endogenous and exogenous spatial information, jointly determining attentional orienting toward the most relevant spatial location.





2018 ◽  
Vol 119 (2) ◽  
pp. 476-489 ◽  
Author(s):  
Brian J. Gereke ◽  
Alexandra J. Mably ◽  
Laura Lee Colgin

CA1 place cells become more anticipatory with experience, an effect thought to be caused by NMDA receptor-dependent plasticity in the CA3–CA1 network. Theta (~5–12 Hz), slow gamma (~25–50 Hz), and fast gamma (~50–100 Hz) rhythms are thought to route spatial information in the hippocampal formation and to coordinate place cell ensembles. Yet, it is unknown whether these rhythms exhibit experience-dependent changes concurrent with those observed in place cells. Slow gamma rhythms are thought to indicate inputs from CA3 to CA1, and such inputs are thought to be strengthened with experience. Thus, we hypothesized that slow gamma rhythms would become more evident with experience. We tested this hypothesis using mice freely traversing a familiar circular track for three 10-min sessions per day. We found that slow gamma amplitude was reduced in the early minutes of the first session of each day, even though both theta and fast gamma amplitudes were elevated during this same period. However, in the first minutes of the second and third sessions of each day, all three rhythms were elevated. Interestingly, theta was elevated to a greater degree in the first minutes of the first session than in the first minutes of later sessions. Additionally, all three rhythms were strongly influenced by running speed in dynamic ways, with the influence of running speed on theta and slow gamma changing over time within and across sessions. These results raise the possibility that experience-dependent changes in hippocampal rhythms relate to changes in place cell activity that emerge with experience. NEW & NOTEWORTHY We show that CA1 theta, slow gamma, and fast gamma rhythms exhibit characteristic changes over time within sessions in familiar environments. These effects in familiar environments evolve across repeated sessions.



2014 ◽  
Vol 369 (1635) ◽  
pp. 20120516 ◽  
Author(s):  
Sheng-Jia Zhang ◽  
Jing Ye ◽  
Jonathan J. Couey ◽  
Menno Witter ◽  
Edvard I. Moser ◽  
...  

The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. We have developed an optogenetic strategy to identify functionally defined cell types in the MEC that project directly to the hippocampus. By expressing channelrhodopsin-2 (ChR2) selectively in the hippocampus-projecting subset of entorhinal projection neurons, we were able to use light-evoked discharge as an instrument to determine whether specific entorhinal cell groups—such as grid cells, border cells and head-direction cells—have direct hippocampal projections. Photoinduced firing was observed at fixed minimal latencies in all functional cell categories, with grid cells as the most abundant hippocampus-projecting spatial cell type. We discuss how photoexcitation experiments can be used to distinguish the subset of hippocampus-projecting entorhinal neurons from neurons that are activated indirectly through the network. The functional breadth of entorhinal input implied by this analysis opens up the potential for rich dynamic interactions between place cells in the hippocampus and different functional cell types in the entorhinal cortex (EC).



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