Oscillatory neurocomputing with ring attractors: a network architecture for mapping locations in space onto patterns of neural synchrony

Theories of neural coding seek to explain how states of the world are mapped onto states of the brain. Here, we compare how an animal''s location in space can be encoded by two different kinds of brain states: population vectors stored by patterns of neural firing rates, versus synchronization vectors stored by patterns of synchrony among neural oscillators. It has previously been shown that a population code stored by spatially tuned ‘grid cells’ can exhibit desirable properties such as high storage capacity and strong fault tolerance; here it is shown that similar properties are attainable with a synchronization code stored by rhythmically bursting ‘theta cells’ that lack spatial tuning. Simulations of a ring attractor network composed from theta cells suggest how a synchronization code might be implemented using fewer neurons and synapses than a population code with similar storage capacity. It is conjectured that reciprocal connections between grid and theta cells might control phase noise to correct two kinds of errors that can arise in the code: path integration and teleportation errors. Based upon these analyses, it is proposed that a primary function of spatially tuned neurons might be to couple the phases of neural oscillators in a manner that allows them to encode spatial locations as patterns of neural synchrony.     

Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations,movement between goals,and environmental context in a radial-arm arena

The amniote hippocampal formation plays an evolutionarily-conserved role in the neural representation of environmental space. However, species differences in spatial ecology nurture the expectation of species differences in how hippocampal neurons represent space. To determine the spatial response properties of homing pigeon (Columba livia) HFneurons, we recorded from isolated units in birds freely navigating a radial arena in search of food present at four goal locations. Fifty of 76 neurons displayed firing rate variations that could be placed into three response categories. Location cells (n=25) displayed higher firing rates at restricted locations in the arena space, often in proximity to goal locations. Path cells (n=13) displayed higher firing rates as a pigeon moved between a subset of goal locations. Arena-off cells (n=12) were more active when a pigeon was in a baseline holding space compared to inside the arena. Overall, reliability and coherence scores of the recorded neurons were lower compared to rat place cells. The differences in the spatial response profiles of pigeon hippocampal formation neurons, when compared to rats, provide a departure point for better understanding the relationship between spatial behavior and how hippocampal formation neurons participate in the representation of space.     

Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.)

It has been hypothesized that individuals who have higher demands for spatially based behaviours should show increases in hippocampal attributes. Some avian species have been shown to use a spatially based representation of their environment during migration. Further, differences in hippocampal attributes have been shown between migratory and non-migratory subspecies as well as between individuals with and without migratory experience (juveniles versus adults). We tested whether migratory behaviour might also be associated with increased hippocampal neurogenesis, and whether potential differences track previously reported differences in hippocampal attributes between a migratory (Zonotrichia leucophrys gambelii) and non-migratory subspecies (Z. l. nuttalli) of white-crowned sparrows. We found that non-migratory adults had relatively fewer numbers of immature hippocampal neurons than adult migratory birds, while adult non-migrants had a lower density of new hippocampal neurons than adult and juvenile migratory birds and juvenile non-migratory birds. Our results suggest that neurogenesis decreases with age, as juveniles, regardless of migratory status, exhibit similar and higher levels of neurogenesis than non-migratory adults. However, our results also suggest that adult migrants may either seasonally increase or maintain neurogenesis levels comparable to those found in juveniles. Our results thus suggest that migratory behaviour in adults is associated with maintained or increased neurogenesis and the differential production of new neurons may be the mechanism underpinning changes in the hippocampal architecture between adult migratory and non-migratory birds.     

Dissociation of exteroceptive and idiothetic orientation cues: effect on hippocampal place cells and place navigation.

Navigation by means of cognitive maps appears to require the hippocampus; hippocampal place cells (PCs) appear to store spatial memories because their discharge is confined to cell-specific places called firing fields (FFs). Experiments with rats manipulated idiothetic and landmark-related information to understand the relationship between PC activity and spatial cognition. Rotating a circular arena in the light caused a discrepancy between these cues. This discrepancy caused most FFs to disappear in both the arena and room reference frames. However, FFs persisted in the rotating arena frame when the discrepancy was reduced by darkness or by a card in the arena. The discrepancy was increased by ''field clamping'' the rat in a room-defined FF location by rotations that countered its locomotion. Most FFs dissipated and reappeared an hour or more after the clamp. Place-avoidance experiments showed that navigation uses independent idiothetic and exteroceptive memories. Rats learned to avoid the unmarked footshock region within a circular arena. When acquired on the stable arena in the light, the location of the punishment was learned by using both room and idiothetic cues; extinction in the dark transferred to the following session in the light. If, however, extinction occurred during rotation, only the arena-frame avoidance was extinguished in darkness; the room-defined location was avoided when the lights were turned back on. Idiothetic memory of room-defined avoidance was not formed during rotation in light; regardless of rotation, there was no avoidance when the lights were turned off, but room-frame avoidance reappeared when the lights were turned back on. The place-preference task rewarded visits to an allocentric target location with a randomly dispersed pellet. The resulting behaviour alternated between random pellet searching and target-directed navigation, making it possible to examine PC correlates of these two classes of spatial behaviour. The independence of idiothetic and exteroceptive spatial memories and the disruption of PC firing during rotation suggest that PCs may not be necessary for spatial cognition; this idea can be tested by recordings during the place-avoidance and preference tasks.     

Elucidating the significance of spatial memory on movement decisions by African savannah elephants using state–space models

Spatial memory facilitates resource acquisition where resources are patchy, but how it influences movement behaviour of wide-ranging species remains to be resolved. We examined African elephant spatial memory reflected in movement decisions regarding access to perennial waterholes. State–space models of movement data revealed a rapid, highly directional movement behaviour almost exclusively associated with visiting perennial water. Behavioural change point (BCP) analyses demonstrated that these goal-oriented movements were initiated on average 4.59 km, and up to 49.97 km, from the visited waterhole, with the closest waterhole accessed 90% of the time. Distances of decision points increased when switching to different waterholes, during the dry season, or for female groups relative to males, while selection of the closest waterhole decreased when switching. Overall, our analyses indicated detailed spatial knowledge over large scales, enabling elephants to minimize travel distance through highly directional movement when accessing water. We discuss the likely cognitive and socioecological mechanisms driving these spatially precise movements that are most consistent with our findings. By applying modern analytic techniques to high-resolution movement data, this study illustrates emerging approaches for studying how cognition structures animal movement behaviour in different ecological and social contexts.     

Optical imaging of odorant representations in the mammalian olfactory bulb.

We adapted the technique of intrinsic signal imaging to visualize how odorant concentration and structure are represented spatially in the rat olfactory bulb. Most odorants activated one or more glomeruli in the imaged region of the bulb; these optically imaged responses reflected the excitation of underlying neurons. Odorant-evoked patterns were similar across animals and symmetrical in the two bulbs of the same animal. The variable sensitivity of individual glomeruli produced distinct maps for different odorant concentrations. Using a series of homologous aldehydes, we found that glomeruli were tuned to detect particular molecular features and that maps of similar molecules were highly correlated. These characteristics suggest that odorants and their concentrations can be encoded by distinct spatial patterns of glomerular activation.     

Key Features of Human Episodic Recollection in the Cross-Episode Retrieval of Rat Hippocampus Representations of Space

Neurophysiological studies focus on memory retrieval as a reproduction of what was experienced and have established that neural discharge is replayed to express memory. However, cognitive psychology has established that recollection is not a verbatim replay of stored information. Recollection is constructive, the product of memory retrieval cues, the information stored in memory, and the subject''s state of mind. We discovered key features of constructive recollection embedded in the rat CA1 ensemble discharge during an active avoidance task. Rats learned two task variants, one with the arena stable, the other with it rotating; each variant defined a distinct behavioral episode. During the rotating episode, the ensemble discharge of CA1 principal neurons was dynamically organized to concurrently represent space in two distinct codes. The code for spatial reference frame switched rapidly between representing the rat''s current location in either the stationary spatial frame of the room or the rotating frame of the arena. The code for task variant switched less frequently between a representation of the current rotating episode and the stable episode from the rat''s past. The characteristics and interplay of these two hippocampal codes revealed three key properties of constructive recollection. (1) Although the ensemble representations of the stable and rotating episodes were distinct, ensemble discharge during rotation occasionally resembled the stable condition, demonstrating cross-episode retrieval of the representation of the remote, stable episode. (2) This cross-episode retrieval at the level of the code for task variant was more likely when the rotating arena was about to match its orientation in the stable episode. (3) The likelihood of cross-episode retrieval was influenced by preretrieval information that was signaled at the level of the code for spatial reference frame. Thus key features of episodic recollection manifest in rat hippocampal representations of space.     

Spatial learning and action planning in a prefrontal cortical network model

The interplay between hippocampus and prefrontal cortex (PFC) is fundamental to spatial cognition. Complementing hippocampal place coding, prefrontal representations provide more abstract and hierarchically organized memories suitable for decision making. We model a prefrontal network mediating distributed information processing for spatial learning and action planning. Specific connectivity and synaptic adaptation principles shape the recurrent dynamics of the network arranged in cortical minicolumns. We show how the PFC columnar organization is suitable for learning sparse topological-metrical representations from redundant hippocampal inputs. The recurrent nature of the network supports multilevel spatial processing, allowing structural features of the environment to be encoded. An activation diffusion mechanism spreads the neural activity through the column population leading to trajectory planning. The model provides a functional framework for interpreting the activity of PFC neurons recorded during navigation tasks. We illustrate the link from single unit activity to behavioral responses. The results suggest plausible neural mechanisms subserving the cognitive "insight" capability originally attributed to rodents by Tolman & Honzik. Our time course analysis of neural responses shows how the interaction between hippocampus and PFC can yield the encoding of manifold information pertinent to spatial planning, including prospective coding and distance-to-goal correlates.     

Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields

The receptive field (RF) of single visual neurons undergoes progressive refinement during development. It remains largely unknown how the excitatory and inhibitory inputs on single developing neurons are refined in a coordinated manner to allow the formation of functionally correct circuits. Using whole-cell voltage-clamp recording from Xenopus tectal neurons, we found that RFs determined by excitatory and inhibitory inputs in more mature tectal neurons are spatially matched, with each spot stimulus evoking balanced synaptic excitation and inhibition. This emerges during development through a gradual reduction in the RF size and a transition from disparate to matched topography of excitatory and inhibitory inputs to the tectal neurons. Altering normal spiking activity of tectal neurons by either blocking or elevating GABA(A) receptor activity significantly impeded the developmental reduction and topographic matching of RFs. Thus, appropriate inhibitory activity is essential for the coordinated refinement of excitatory and inhibitory connections.     

Play behaviour in group-housed dairy calves, the effect of space allowance

In dairy calves kept in pens, lack of sufficient space may inhibit the performance of play behaviour. The present study investigated, firstly, if an increase in space allowance increases the occurrence of play behaviour, and secondly, if calves kept at a low space allowance perform more locomotor play when released individually in a large novel area. A total of 96 dairy calves in six repetitions were housed in groups of four, in pens of either 4, 3, 2.2 or 1.5 m(2) per calf from 2 weeks of age. The occurrence of play behaviour in the home environment was recorded continuously for each individual calf during 24 h at 5, 7 and 9 weeks of age. Locomotor play decreased over the weeks (54, 29 and 19 s for weeks 5, 7 and 9, respectively; F(2,40)=17.98; P<0.001), and the interaction between space allowance and week tended to be significant (F(6,40)=1.96; P<0.10). At 5 weeks of age, calves kept at 4 or 3 m(2) per calf performed more locomotor play in the home environment than calves at 2.2 or 1.5 m(2) per calf (68, 74, 38 and 39 s for 4, 3, 2.2 and 1.5 m(2) per calf, respectively; F(3,15)=3.40; P<0.05), but in weeks 7 and 9, no effects of space allowance were found. In addition, the duration of locomotor play was recorded for all calves during an individual 10-min open-field test in a 9.6x4.8 m arena at 4 and 10 weeks of age. During the open-field test at 10 weeks of age, calves from pens with 1.5 m(2) per calf performed more locomotor play than calves on the remaining treatments (10, 9, 12 and 25 s for 4, 3, 2.2 and 1.5 m(2) per calf, respectively; F(3,15)=4.05; P<0.05). The present study shows that an increase in the available space increases the occurrence of locomotor play in the home environment at 5 weeks of age. It also shows that calves kept in pens with the smallest space allowance performed more locomotor play behaviour when released in a large arena at 10 weeks of age.     

The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms

Emerging evidence suggests that a group of dietary-derived phytochemicals known as flavonoids are able to induce improvements in memory, learning and cognition. Flavonoids have been shown to modulate critical neuronal signalling pathways involved in processes of memory, and therefore are likely to affect synaptic plasticity and long-term potentiation mechanisms, widely considered to provide a basis for memory. Animal dietary supplementation studies have further shown that flavonoid-rich foods are able to reverse age-related spatial memory and spatial learning impairments. A more accurate understanding of how a particular spatial memory task works and of which aspects of memory and learning can be assessed in each case, are necessary for a correct interpretation of data relating to diet-cognition experiments. Further understanding of how specific behavioural tasks relate to the functioning of hippocampal circuitry during learning processes might be also elucidative of the specific observed memory improvements. The overall goal of this review is to give an overview of how the hippocampal circuitry operates as a memory system during behavioural tasks, which we believe will provide a new insight into the underlying mechanisms of the action of flavonoids on cognition.     

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

 A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learning is applied to map place cell activity into action cell activity. The ensemble action cell activity provides navigational maps to support spatial behavior. We present experimental results obtained with a mobile Khepera robot. Received: 02 July 1999 / Accepted in revised form: 20 March 2000     

Changes in the rhesus mother-infant relationship through the first four months of life

Measurements of the course of interactions between rhesus monkey infants (Macaca mulatta) and their mothers during the infant's first 16 weeks showed changes in the tendencies of both partners to be together and apart. Referring only to the partner who was primarily responsible for an age-related change, by using a single index of responsibility for contact or proximity, was found to be an oversimplification. Maternal rejecting behaviour may have been primarily responsible for changes in the time spent apart only during the first 6 weeks. After the infants' sixth week, both partners' tendencies to be apart increased together. Infants then began to spend longer away partly to interact with social companions other than their mother. Mothers restricted and followed their infants more up to week 4, but after week 8 decreases in these measures allowed infants to spend longer away. Similarities between the time courses of the time spent apart from their mothers by rhesus infants in this study and in field studies are pointed out. The similarities seem striking partly because differences between studies that do not use confidence intervals (or standard errors) cannot be shown easily. Conflict between parent and infant occurred, but how it appears, and how significant it is in each species at each infant age, remains to be discovered.     

Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds

Maintaining cognitive processes comes with neurological costs. Thus, enhanced cognition and its underlying neural mechanisms should change in response to environmental pressures. Indeed, recent evidence suggests that variation in spatially based cognitive abilities is reflected in the morphology of the hippocampus (Hp), the region of the brain involved in spatial memory. Moreover, recent work on this region establishes a dynamic link between brain plasticity and cognitive experiences both across populations and within individuals. However, the mechanisms involved in neurological changes as a result of differential space use and the reversibility of such effects are unknown. Using a house sparrow (Passer domesticus ) model, we experimentally manipulated the space available to birds, testing the hypothesis that reductions in dendritic branching is associated with reduced Hp volume and that such reductions in volume are reversible. We found that reduced spatial availability associated with captivity had a profound and significant reduction in sparrow hippocampal volumes, which was highly correlated with the total length of dendrites in the region. This result suggests that changes to the dendritic structure of neurons may, in part, explain volumetric reductions in region size associated with captivity. In addition, small changes in available space even within captivity produced significant changes in the spine structure on Hp dendrites. These reductions were reversible following increased spatial opportunities. Overall, these results are consistent with the hypothesis that reductions to the Hp in captivity, often assumed to reflect a deleterious process, may be adaptive and a consequence of the trade‐off between cognitive and energetic demands. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 93–101, 2017     

Explanations for variation in cognitive ability: Behavioural ecology meets comparative cognition

Sara Shettleworth has played a defining role in the development of animal cognition and its integration into other parts of biology, especially behavioural ecology. Here we chart some of that progress in understanding the causes and importance of variation in cognitive ability and highlight how Tinbergen's levels of explanation provide a useful framework for this field. We also review how experimental design is crucial in investigating cognition and stress the need for naturalistic experiments and field studies. We focus particularly on the example of the relationship among food hoarding, spatial cognition and hippocampal structure, and review the conflicting evidence for sex differences in spatial cognition. We finish with speculation that a combination of Tinbergen and Shettleworth-style approaches would be the way to grapple with the as-yet unanswered questions of why birds mimic heterospecifics.     

高脂饲养青春期大鼠电击回避反应和海马CA3区场电位的改变

目的：观察高脂饲养至青春期的大鼠对电击回避反应和海马CA3区实时局部场电位变化。方法：断乳1周幼鼠改用基础饲料和高脂饲料分别喂养4周至青春期,分为基础饲料组（BF组）和高脂饲料组（HFD组）,Y型迷宫电击回避训练方法,记录2组大鼠电击回避达学会标准的相关参数,同时无线遥测大鼠达标时海马CA3区实时局部场电位。结果：与BF组大鼠比较,HFD组大鼠体重明显增加,Y型迷宫电击回避训练1~2 d大鼠达标百分率、电击回避达标各项指标均略优于BF组;双侧海马CA3区局部场电位节律出现去同步化快波改变,右侧海马CA3区出现了θ波和γ 1波百分比的同步性增加,但无θ~γ 1波相位-振幅耦合出现。结论：幼年期短期高脂饮食至青春期的大鼠,尽管体重较基础饲料大鼠增加,但未见Y型迷宫电击回避反应能力和海马依赖性空间认知功能的减退。     

Sharp wave/ripple network oscillations and learning-associated hippocampal maps

Sharp wave/ripple (SWR, 150–250 Hz) hippocampal events have long been postulated to be involved in memory consolidation. However, more recent work has investigated SWRs that occur during active waking behaviour: findings that suggest that SWRs may also play a role in cell assembly strengthening or spatial working memory. Do such theories of SWR function apply to animal learning? This review discusses how general theories linking SWRs to memory-related function may explain circuit mechanisms related to rodent spatial learning and to the associated stabilization of new cognitive maps.     

早期声音暴露对蝙蝠中脑下丘听神经元频率调谐特性发育的影响

本实验对鼠耳蝠出生后不同时期进行纯音暴露,采用常规电生理不方法研究出生后早期声音暴露出蝙蝠中脑下丘听神经元频率调谐特性发育的影响及影响的临界期。结果表明,出生后第１,３周开始声暴露的实验组,其神经元调于暴露声频段的数量较对照组和出生后第５周开始声暴露的实验组明显增多,且音调筑构出现扭曲,神经元频率调谐曲线的Ｑ１０－ｄＢ值也较高。     

Adolescent development of neuron structure in dentate gyrus granule cells of male Syrian hamsters

Hippocampal function, including spatial cognition and stress responses, matures during adolescence. In addition, hippocampal neuron structure is modified by gonadal steroid hormones, which increase dramatically at this time. This study investigated pubertal changes in dendritic complexity of dentate gyrus neurons. Dendrites, spines, and cell bodies of Golgi-impregnated neurons from the granule cell layer were traced in pre-, mid-, and late-pubertal male Syrian hamsters (21, 35, and 49 days of age). Sholl analysis determined the number of intersections and total dendritic length contained in concentric spheres set at 25-microm increments from the soma. Spine densities were quantified separately in proximal and distal segments of a subset of neurons used for the Sholl analysis. We found that the structure of neurons in the lower, but not upper, blade of the dentate gyrus changed during adolescence. The lower, infrapyramidal blade showed pruning of dendrites close to the cell body and increases in distal dendritic spine densities across adolescence. These data demonstrate that dentate gyrus neurons undergo substantial structural remodeling during adolescence and that patterns of maturation are region specific. Furthermore, these changes in dendrite structure, which alter the electrophysiological properties of granule cells, are likely related to the adolescent development of hippocampal-dependent cognitive functions such as learning and memory, as well as hippocampus-mediated stress responsivity.