Neural basis of the spatial navigation based on geometric cues

Recent studies have found that hippocampus of mammals and birds and the lateral pallium of the fish telencephalon are critical for learning the geometric properties of space. Nevertheless, other studies suggest that navigation based on geometric information is primarily supported by proximal cues near the target location. According to this hypothesis, animals could use a taxon strategy to navigate an environment where only geometric cues are available and the results from lesion studies could be masking other effects related to the use of featural information. In the present study, we examined the effects of lesions to the lateral pallium of goldfish in the encoding of geometric spatial information. Goldfish with telencephalic lesions were trained to search for a goal in a rectangular-shaped arena with either one or two possible goals. Lateral pallium lesions do not interfere with goal location when the geometric information defined the goal unambiguously. Present results suggest that the geometric information is sensitive to be encoded in taxon strategies and therefore it could not depend directly on the correct functioning of the hippocampal system.     

Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish

The forebrain of vertebrates shows great morphological variation and specialized adaptations. However, an increasing amount of neuroanatomical and functional data reveal that the evolution of the vertebrate forebrain could have been more conservative than previously realized. For example, the pallial region of the teleost telencephalon contains subdivisions presumably homologous with various pallial areas in amniotes, including possibly a homologue of the medial pallium or hippocampus. In mammals and birds, the hippocampus is critical for encoding complex spatial information to form map-like cognitive representations of the environment. Here, we present data showing that the pallial areas of reptiles and fish, previously proposed as homologous to the hippocampus of mammals and birds on an anatomical basis, are similarly involved in spatial memory and navigation by map-like or relational representations of the allocentric space. These data suggest that early in vertebrate evolution, the medial pallium of an ancestral fish group that gave rise to the extant vertebrates became specialized for processing and encoding complex spatial information, and that this functional trait has been retained through the evolution of each independent vertebrate lineage.     

Hallmarks of a common forebrain vertebrate plan: specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish

In mammals and birds different pallial forebrain areas participate in separate memory systems. In particular, the hippocampal pallium is implicated in spatial memory and temporal attribute processing, whereas the amygdalar pallium is involved in emotional memory. Here we analyze the involvement of teleost fish lateral and medial pallia, proposed as homologous to the hippocampus and amygdala, respectively, in a variety of learning and memory tasks, such as spatial memory; reversal learning; delay or trace motor classical conditioning; heart rate, emotional classical conditioning; and two way active avoidance conditioning. Results show that the damage to the lateral pallium produces a profound deficit in spatial learning and memory in teleost fish. In addition, lateral pallium lesions produce a significant deficit in trace classical conditioning, whereas they have no significant effects on delay conditioning, or in heart rate conditioning. In contrast, medial pallium lesions disrupt emotional, heart rate conditioning and avoidance conditioning, but spare spatial memory and temporal stimulus processing. These data demonstrate a striking functional similarity between the medial and lateral pallia of teleost fish and the pallial amygdala and hippocampal pallium of land vertebrates, respectively. The reviewed evidence suggest that these two separate memory systems, the hippocampus-dependent spatial, relational or temporal memory system, and the amygdala based emotional memory system, could have appeared early during evolution, having conserved their functional identity through vertebrate phylogenesis.     

Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems

In mammals, the amygdala and the hippocampus are involved in different aspects of learning. Whereas the amygdala complex is involved in emotional learning, the hippocampus plays a critical role in spatial and contextual learning. In fish, it has been suggested that the medial and lateral region of the telencephalic pallia might be the homologous neural structure to the mammalian amygdala and hippocampus, respectively. Although there is evidence of the implication of medial and lateral pallium in several learning processes, it remains unclear whether both pallial areas are involved distinctively in different learning processes. To address this issue, we examined the effect of selective ablation of the medial and lateral pallium on both two-way avoidance and reversal spatial learning in goldfish. The results showed that medial pallium lesions selectively impaired the two-way avoidance task. In contrast, lateral pallium ablations impaired the spatial task without affecting the avoidance performance. These results indicate that the medial and lateral pallia in fish are functionally different and necessary for emotional and spatial learning, respectively. Present data could support the hypothesis that a sketch of these regions of the limbic system, and their associated functions, were present in the common ancestor of fish and terrestrial vertebrates 400 million years ago.     

The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish

In mammals, the pallial amygdala is implicated in emotional learning and memory, whereas the hippocampus is involved in spatial, contextual, or relational memory. This review presents a set of experiments aimed to study the involvement of the dorsomedial and dorsolateral telencephalon of goldfish in spatial and active avoidance learning. Results showed that (1) medial lesions impaired both acquisition and retention of conditioned avoidance response in two-way active avoidance learning experiments with stimuli overlapping (emotional factor) and with an interstimuli gap (temporal and emotional factors), and (2) the medial lesion did not affect spatial learning (spatial, contextual, or relational factors). In contrast, lateral lesions did not impair conditioned avoidance response with stimuli overlapping, but affected conditioned avoidance response with an interstimuli gap and spatial learning. These results support the presence of two differentiated memory systems in teleost fish based on discrete pallial regions: emotional (dorsomedial telencephalon) and spatial/temporal or relational (dorsolateral telencephalon). Furthermore, these functional data support the homology between the medial pallium of the teleost and the pallial amygdala of land vertebrates, and between the teleost lateral pallium and the mammalian hippocampus.     

Spatial and non-spatial learning in turtles: the role of medial cortex

In mammals and birds, hippocampal processing is crucial for allocentric spatial learning. In these vertebrate groups, lesions to the hippocampal formation produce selective impairments in spatial tasks that require the encoding of relationships among environmental features, but not in tasks that require the approach to a single cue or simple non-spatial discriminations. In reptiles, a great deal of anatomical evidence indicates that the medial cortex (MC) could be homologous to the hippocampus of mammals and birds; however, few studies have examined the functional role of this structure in relation to learning and memory processes. The aim of this work was to study how the MC lesions affect spatial strategies. Results of Experiment 1 showed that the MC lesion impaired the performance in animals pre-operatively trained in a place task, and although these animals were able to learn the same task after surgery, probe test revealed that learning strategies used by MC lesioned turtles were different to that observed in sham animals. Experiment 2 showed that the MC lesion did not impair the retention of the pre-operatively learned task when a single intramaze visual cue identified the goal. These results suggest that the reptilian MC and hippocampus of mammals and birds function in quite similar ways, not only in relation to those spatial functions that are impaired, but also in relation to those learning processes that are not affected.     

The evolution of the cognitive map

The hippocampal formation of mammals and birds mediates spatial orientation behaviors consistent with a map-like representation, which allows the navigator to construct a new route across unfamiliar terrain. This cognitive map thus appears to underlie long-distance navigation. Its mediation by the hippocampal formation and its presence in birds and mammals suggests that at least one function of the ancestral medial pallium was spatial navigation. Recent studies of the goldfish and certain reptile species have shown that the medial pallium homologue in these species can also play an important role in spatial orientation. It is not yet clear, however, whether one type of cognitive map is found in these groups or indeed in all vertebrates. To answer this question, we need a more precise definition of the map. The recently proposed parallel map theory of hippocampal function provides a new perspective on this question, by unpacking the mammalian cognitive map into two dissociable mapping processes, mediated by different hippocampal subfields. If the cognitive map of non-mammals is constructed in a similar manner, the parallel map theory may facilitate the analysis of homologies, both in behavior and in the function of medial pallium subareas.     

What are the functions of fish brain pallium?

There is some experimental evidence that the pallial areas of a fish's brain are involved in distincted learning functions. Recently published data suggest that the medial pallium is essential for avoidance learning and the lateral pallium is crucial for spatial learning and is also involved in temporal aspects of the learning processes. This data joined to the proposal of homologies between medial and lateral fish pallia and pallial amygdala and hippocampus respectively, suggest that the pallial areas could have preserved their functions throughout vertebrates’ evolution. However, the functional implication of dorsal pallium that has been proposed as homologous to mammalian isocortex and transition cortex is largely unknown. In this study we analyze the role of dorsal pallium in trace and non-trace avoidance learning. Our results show the implication of this area in trace conditioning, but not in non-trace conditioning. This result allows discussion of homology proposals among lateral, dorsal, and medial pallia and hippocampus, isocortex, and pallial amygdala respectively.     

Effects of medial and dorsal cortex lesions on spatial memory in lizards

In mammals and birds, the hippocampus is a major learning and memory center that plays a prominent role in spatial memory, the use of distal cues to guide navigation. The role of reptilian hippocampal homologues, the medial and dorsal cortex, in spatial memory has not been thoroughly investigated. The medial and dorsal cortex of reptiles is known to play a role in learning both tasks that are hippocampally dependent and tasks that are not hippocampally dependent in mammals and birds. In order to examine the specific role of the medial and dorsal cortex in spatial memory, we trained medial cortex, dorsal cortex, and sham lesioned Cnemidophorus inornatus lizards to locate the one heated rock of four identical rocks spaced evenly around the perimeter of a circular, sand filled, arena in a cool room. We used probe trials to examine the strategies used by lizards to locate the goal. Medial cortex lesions and dorsal cortex lesions slowed acquisition and altered the strategies used to locate the goal. However, none of the lizards adopted a spatial strategy to locate the goal suggesting that the dorsal cortex and medial cortex are involved in using non-spatial strategies for navigation.     

A reduced progenitor pool population accounts for the rudimentary appearance of the septum, medial pallium and dorsal pallium in birds

To date, most studies comparing birds and mammals have focused on the similarities in brain development, architecture and connectivity. However, major differences in size, anatomy and organization exist in the telencephalon of adult birds and mammals. For instance, the septum, medial pallium and dorsal pallium of birds appear rudimentary compared with those of mammals. To identify the developmental processes that give rise to this difference in size and anatomy of the septum, medial pallium and dorsal pallium, the thickness of the ventricular zone that encompasses these regions was measured in embryonic birds (i.e. chickens, sparrows) and mammals (i.e. rabbits, hedgehogs, shrews, platypus). Cumulative bromodeoxyuridine (BrdU) labeling in chickens at embryonic day 7 and 8 was also used to examine levels of cell proliferation in the ventricular zone of the septum, medial pallium and dorsal pallium. The study's main finding is that the ventricular zone of the septum, medial pallium and dorsal pallium is thinner in birds than in mammals. In chickens, the septum, medial pallium and dorsal pallium ventricular zone harbor few proliferating (i.e. BrdU+) cells. Collectively, these findings suggest that a reduced progenitor pool population account for the 'rudimentary' appearance of the avian septum, medial pallium and dorsal pallium.     

Is the avian hippocampus a functional homologue of the mammalian hippocampus?

The effects of hippocampal lesions on the processing and retention of visual and spatial information in birds and mammals is reviewed. Both birds and mammals with damage to the hippocampus are severely impaired on a variety of spatial tasks, such as navigation, maze learning, and the retention of spatial information. In contrast, both birds and mammals with damage to the hippocampus are not impaired on a variety of visual tasks, such as delayed matching-to-sample, concurrent discrimination, or retention of a visual discrimination. In addition, both birds and mammals with hippocampal damage display impairments in the acquisition of an autoshaped response, as well as alterations in response suppression. These findings suggest that the avian hippocampus is a functional homologue of the mammalian hippocampus, and that in both birds and mammals the hippocampus is important for the processing and retention of spatial, rather than purely visual information.     

Cognitive and emotional functions of the teleost fish cerebellum

Increasing experimental and neuropsychological evidence indicates that the cerebellum of humans and other mammals, traditionally associated with motor control, is implicated in a variety of cognitive and emotional functions. For example, the cerebellum has been identified as an essential structure in different learning processes, ranging from simple forms of associative, sensory-motor learning and emotional conditioning, to more complex, higher-order processes such as spatial cognition. Although neuroanatomical and neurophysiological data indicate that the organization of the cerebellum is notably well conserved in vertebrates, little is actually known about the cerebellar contribution to processes besides the motor domain in non-mammals. In this work, we analyzed the involvement of the teleost fish cerebellum on classical conditioning of motor and emotional responses and on spatial cognition. Cerebellum lesions in goldfish impair the classical conditioning of a simple eye-retraction response analogous to the eyeblink conditioning described in mammals. Single unit extracellular electrophysiological recording and cytochrome oxidase histochemistry also reveal the involvement of the teleost fish cerebellum in classical conditioning. Autonomic emotional responses (e.g., heart rate classical conditioning) are also impaired by cerebellum lesions in goldfish. Furthermore, goldfish with cerebellum lesions present a severe impairment in spatial cognition. In contrast, cerebellum lesions do not produce any observable motor deficit as indicated by the swimming activity or obstacle avoidance and do not interfere with the occurrence of unconditioned motor or emotional responses. These data indicate that the functional involvement of the teleost cerebellum in learning and memory is strikingly similar to mammals and suggest that the cognitive and emotional functions of the cerebellum may have evolved early in vertebrate evolution, having been conserved along the phylogenetic history of the extant vertebrate groups.     

Understanding the basic circuitry of the cerebral hemispheres: the case of lizards and its implications in the evolution of the telencephalon

The organization of the cerebral hemispheres of mammals is characterized by corticostriatal glutamatergic projections and striatopallidal GABAergic ones, plus the descending projections of the pallium and subpallium to extratelencephalic targets. The present review of the available neuroanatomical data on the forebrain of lizards suggests that the telencephalon of reptiles also follows this basic pattern of connectivity. In addition, we show that this basic circuitry includes a pallido-cortical projection, therefore forming a cortico-striato-pallido-cortical circuit. The analysis of this circuitry for the medial, dorsal, lateral, and ventral pallial divisions in reptiles and mammals leads to the following conclusions: (1) The medial and dorsal cortices of lizards together appear to be equivalent to the medial pallium of mammals. (2) The projection from the lacertilian dorsal cortex to the striatum proper resembles the subiculo-striatal projection of mammals, rather than the isocortical projection to the caudatus-putamen. (3) Most of the dorsal striatum of reptiles is engaged in the corticostriatal circuit corresponding to the ventral pallium (the anterior dorsal ventricular ridge), and therefore, it is not equivalent to the mammalian caudatus-putamen, which is involved in the circuit of the dorsal pallium. (4) The main and accessory olfactory bulbs also follow this pattern of connections.     

Parallel information processing in the dorsal striatum: relation to hippocampal function.

We investigated the effects of localized medial and lateral CPu lesions and fornix/fimbria lesions on responses to a local cue and to behavior based on cognitive-spatial information in the water maze. Rats were trained concurrently on the cue (visible platform) and spatial (submerged platform) components of the task, followed by a test in which responses to the two types of information were dissociated by a measure of competing response tendencies. Bilateral lesions of lateral CPu did not affect acquisition of either cue or spatial responding but produced a preference for the spatial response on the competition test. Bilateral lesions of the medial CPu retarded but did not prevent learning both components and produced a preference for the cue response on the competition test. The latter effect was accompanied by increased thigmotaxis (swimming in the periphery of the pool), primarily during the early acquisition trials, which was attributed to an impaired ability to respond to learned spatial information. Fornix/fimbria lesions prevented spatial but not cue learning and produced a preference for the cue response on the competition test. Asymmetric lesions (unilateral hippocampus and contralateral medial CPu) produced mild retardation of acquisition of both the cue and spatial tasks and a preference for the cue response on the competition test. These findings dissociate the functions of the lateral and medial CPu and suggest that the hippocampus and medial CPu may be parts of a system that promotes responding based on learned cognitive-spatial information, particularly in competitive cue-place response situations.     

Connections of the lateral and medial divisions of the goldfish telencephalic pallium

Biotinylated dextran amine and fluorescent carbocyanine dye (DiI) were used to examine connections of the lateral (Dl) and medial (Dm) divisions of the goldfish pallium. Besides numerous intrinsic telencephalic connections to Dl and Dm, major ascending projections to these pallial divisions arise in the preglomerular complex of the posterior tuberculum, rather than in the dorsal thalamus. The rostral subnucleus of the lateral preglomerular nucleus receives auditory input via the medial pretoral nucleus, lateral line input via the ventrolateral toral nucleus, and visual input via the optic tectum, and it projects to both Dl and Dm. The anterior preglomerular nucleus and caudal subnucleus of the lateral preglomerular nucleus receive auditory input via the central toral nucleus and project to Dm. This pallial division also receives chemosensory information via the medial preglomerular nucleus. The central posterior (CP) nucleus, which receives both auditory and visual inputs, also projects to Dm and is the only dorsal thalamic nucleus projecting to the pallium. Thus, both Dl and Dm clearly receive multisensory inputs. Major projections of CP and projections of all other dorsal thalamic nuclei are to the subpallium, however. Descending projections of Dl are primarily to the preoptic area and the caudal hypothalamus, whereas descending projections of Dm are more extensive and particularly heavy to the anterior tuber and nucleus diffusus of the hypothalamus. The topography and connections of Dl are remarkably similar to those of the hippocampus of tetrapods, whereas the topography and connections of Dm are similar to those of the amygdala.     

The ascending tectofugal visual system in amniotes: new insights

Ascending tectal axons carrying visual information constitute a fiber pathway linking the mesencephalon with the dorsal thalamus and then with a number of telencephalic centers. The sauropsidian nucleus rotundus and its mammalian homologue(s) occupy a central position in this pathway. The aim of this study was analyzing the rotundic connections in reptiles and birds in relation with comparable connections in mammals, by using biotinylated dextran amines and the lipophilic carbocyanine dye DiI as tracing molecules. In general, rotundic connections in reptiles and birds are quite similar, especially with regards to pretectal and tectal afferences; as a novel finding, we describe varicose fibers arising from nucleus rotundus that reached the developing chick striatum. In addition, this study described the dorsal claustrum as a novel telencephalic target for the suprageniculate nucleus in mammals. Overall, telencephalic projections from the posterior/intralaminar complex of the mammalian thalamus can be compared with the telencephalic projections of the reptilian nucleus rotundus. With the exception of the isocortical connections, the mouse suprageniculate nucleus shares a number of afferent and efferent connections with the sauropsidian nucleus rotundus. Especially significant were the suprageniculate fibers reaching the striatum and then following to reach pallial derivatives such as the lateral amygdala (ventral pallium) and the dorsal claustrum (lateral pallium). These connections can be compared with the rotundic fibers reaching the ventromedial part of the anterior dorsal ventricular ridge in reptiles/entopallium in birds (ventral pallium) and the dorsolateral part of the anterior dorsal ventricular ridge in reptiles (lateral pallium), and probably the mesopallium in birds.     

Organization of thalamic afferents to anterior dorsal ventricular ridge in turtles. I. Projections of thalamic nuclei

Dorsal ventricular ridge (DVR) is a thalamorecipient, subcortical telencephalic structure in reptiles and birds. Although there is a fair amount of information about sources of afferents to DVR, little is known about the relationship of projections from individual thalamic nuclei to the organization of the structure. This study examines the relationship between thalamic projections and both areal and zonal divisions of anterior DVR (ADVR; Balaban,'78a) of emydid turtles with orthograde degeneration, and horseradish peroxidase techniques. Individual thalamic nuclei contribute either a diffuse or a restricted projection to ADVR. Diffuse projections arise primarily from the dorsomedial anterior nucleus. These fine-caliber axons distribute bilaterally over a wide region of the telencephalon via both medial and lateral thalamotelencephalic pathways. The terminal regions include septum, striatum and the medial bank of cortex caudal to the lamina terminalis. In ADVR, the fibers are distributed sparsely in zones 2–4 of dorsal, medial and ventral areas. Restricted projections to ADVR originate in nucleus rotundus, nucleus reuniens and nucleus caudalis. They ascend ipsilaterally in the lateral thalamotelencephalic pathway (lateral forebrain bundle), and enter ADVR rostral to the anterior commissure. Nucleus rotundus projects to zone 4 of dorsal area, nucleus caudalis projects to zones 2–4 of the dorsal division of medial area, and nucleus reuniens projects to zones 2–4 of both the ventral division of medial area and the ventral area. Comparison of these results with thalamotelencephalic projections in mammals suggests that diffuse and restricted thalamic projection systems are a common feature of both groups. Restricted thalamic projections in reptiles, birds and mammals, terminating in anatomically distinct regions, also appear to be associated with different sensory modalities. The significance of diffuse systems is not clear.     

Evolution of neural processing for visual perception in vertebrates

Visual perception requires both visual information and attention. This review compares, across classes of vertebrates, the functional and anatomical characteristics of (a) the neural pathways that process visual information about objects, and (b) stimulus selection pathways that determine the objects to which an animal attends. Early in the evolution of vertebrate species, visual perception was dominated by information transmitted via the midbrain (retinotectal) visual pathway, and attention was probably controlled primarily by a selection network in the midbrain. In contrast, in primates, visual perception is dominated by information transmitted via the forebrain (retinogeniculate) visual pathway, and attention is mediated largely by networks in the forebrain. In birds and nonprimate mammals, both the retinotectal and retinogeniculate pathways contribute critically to visual information processing, and both midbrain and forebrain networks play important roles in controlling attention. The computations and processing strategies in birds and mammals share some strikingly similar characteristics despite over 300 million years of independent evolution and being implemented by distinct brain architectures. The similarity of these functional characteristics suggests that they provide valuable advantages to visual perception in advanced visual systems. A schema is proposed that describes the evolution of the pathways and computations that enable visual perception in vertebrate species.     

Connections of the commissural nucleus of Cajal in the goldfish,with special reference to the topographic organization of ascending visceral sensory pathways

The primary general visceral nucleus of teleosts is called the commissural nucleus of Cajal (NCC). The NCC of goldfish has been divided into the medial (NCCm) and lateral (NCCl) subnuclei that receive inputs from subdiaphragmatic gastrointestinal tract and the posterior pharynx, respectively. Fiber connections of the NCC were examined by tract‐tracing methods in the goldfish Carassius auratus. Tracer injections into the NCC suggested that the NCC projects directly not only to the secondary visceral sensory region in the rhombencephalic isthmus and other brain stem centers, but also to the forebrain, similar to the situations in mammals, birds, and the Nile tilapia. Although fiber connections of the NCCm and NCCl were basically similar, the NCCm was the more important source of ascending general visceral fibers to the forebrain. Topographic organization was recognized regarding projections to the isthmic secondary visceral sensory zone; input from the NCCm is represented in the secondary general visceral sensory nucleus, while input from the NCCl in the lateral edge of the secondary gustatory nucleus. Moreover, specific injections into different regions of the vagal lobe revealed that the dorsomedio–ventrolateral axis of the lobe is represented in the lateromedial axis of the secondary gustatory nucleus. These observations suggest fine topographic organization of ascending visceral sensory pathways to the isthmic secondary centers. It should also be noted that the reception of primary afferents from the posterior pharynx and projections to the secondary gustatory nucleus suggest that the NCCl may be regarded as a gustatory rather than a general visceral sensory structure. J. Comp. Neurol. 523:209–225, 2015. © 2014 Wiley Periodicals, Inc.     

Effects of partial hippocampal lesions by ibotenic acid on repeated acquisition of spatial discrimination in pigeons

Pigeons were trained on a spatial discrimination task using a repeated acquisition procedure. In this procedure, the pigeons were trained to discriminate between the positions of three keys. One of them was designated the correct key. When the subjects reached the criterion, the discrimination task was changed, with one of two previously incorrect keys now being made the correct key. This procedure was repeated at least 15 times. Then, lesions to the whole hippocampus, the medial hippocampus or to the lateral hippocampus were made by injections of ibotenic acid (Experiment 1). Only the subjects with damage to the whole hippocampus showed deficits in learning after the lesions. The deficits were similar to those caused by aspiration lesions /37/. Knife cuts separating the medial and lateral hippocampi were made in Experiment 2. The subjects did not show deficits in the spatial discrimination task after the sections. Although studies of the connectivity in the avian hippocampus suggested functional differences between the medial and lateral hippocampi, the present results show that pigeons can learn spatial discrimination with the medial and lateral parts of hippocampus separated.