Damage To Which Of The Following Brain Areas Disrupts Spatial Learning?
Introduction
The idea that serotonin (5-hydroxytryptamine; 5-HT) is involved in learning and memory has gained traction in recent years, after having first been suggested in the 1980s (Altman and Normile, 1988). Early on pharmacological studies more often than not implicated spatial memory. More recent studies involving advanced methodologies such as neurotransmitter positron emission tomography (PET) and knockout mouse models have connected to link serotonin to spatial retentiveness.
Spatial memory includes the ability to larn the topographical configuration of environments, to locate objects, to recall previously encountered locations, and to navigate within environments. Many twenty-four hours-to-mean solar day activities performed by animals and humans depend on spatial memory. Knowing where one is, where food and water resource are, and how to go to safety are examples of effective use of spatial memories that are essential for fauna survival. Humans depend on their ability to recall the locations of objects in the environment on a daily basis, ranging from retrieving a mobile phone from a bag to making one's style to work and back home (McNamara, 2013).
At a clinical level, the study of spatial retentivity is of particular significance to several neurological disorders such as dementia of the Alzheimer'southward blazon where impairments in spatial noesis are a central feature. In add-on, spatial memory, and particularly the ability to process and remember spatial descriptions of environments, has been linked to certain types of learning disabilities in children (Mammarella et al., 2014).
Functional neuroimaging studies prove that spatial memory is largely mediated past mesial temporal areas (for example, Maguire et al., 1996b, 1997, 1998a,b; Burgess et al., 2001; Hartley et al., 2003), and within these areas, the hippocampus is a fundamental structure for spatial retentiveness. These regions are characterized by high concentration of the five-HT1A receptor binding sites.
Involvement of the 5-HT1A receptor in cognition is undisputed. This receptor subtype has been suggested as a therapeutic target and neural marker of memory deficits (Meneses, 1999; Meneses and Perez-Garcia, 2007; Thomas, 2015). In this review, we argue that the 5-HT1A receptor plays a key role in spatial learning and retention, and we present bear witness to support this proffer. We first consider the correspondence between the neuroanatomy of spatial retention and the 5-HT1A receptor distribution. Nosotros then review studies using diverse experimental methods that have illustrated the role of 5-HT1A receptors in spatial learning and memory.
Neuroanatomy of Spatial Learning and Memory
Enquiry on spatial memory has consistently implicated a hippocampal encephalon network consisting of the hippocampus proper, the parahippocampal cortices, fornix, parietal cortex, anterior thalamic nuclei, frontal cortex, and the striatum. The critical role of the hippocampal system in spatial learning and retention was first highlighted past Brenda Milner's early on observations of "heightened" spatial memory deficits post-obit temporal lobe excision for the relief of epileptic seizures (Milner, 1958, p. 251). Evidence for the importance of the hippocampus system has connected to accumulate, including very recent findings using single-neuron recording in human entorhinal cortex during virtual navigation (Miller et al., 2015). In terms of possible brain mechanisms underlying spatial learning and memory, findings accept indicated that the rat hippocampus contains "place cells," and these cells exhibit location-specific activity (O'Keefe and Dostrovsky, 1971; O'Keefe and Speakman, 1987). This discovery led to the hypothesis that the hippocampus stores a cognitive map of the spatial layout of the environment (O'Keefe and Nadel, 1978). More than iii decades after, in 2005, "grid cells" were found in the rat's entorhinal cortex, which is the main gateway into the hippocampus (Hafting et al., 2005). Filigree cells generate a coordinate organisation that allows exact positioning and pathfinding. Together with other cells in the entorhinal cortex that recognize the direction of the head of the animal and the border of the environment ("head-direction cells"; Taube, 1998), filigree cells form networks with place cells in the hippocampus. Overall this circuitry constitutes a comprehensive positioning system, an inner global positioning system, or GPS, in the brain.
In addition to these prison cell recording studies, lesions and stimulation of the hippocampus in non-human primate (Parkinson et al., 1988; Angeli et al., 1993) and rodents (Morris et al., 1982; Buhot et al., 1991) were shown to impair spatial learning and memory. Similarly, in humans, medial temporal lesions, especially on the right side, have been shown to impair recollect of spatial location of objects (Smith and Milner, 1981, 1989; Pigott and Milner, 1993; Bohbot et al., 1998; Smith et al., 2011), increase spatial memory errors (using the None-Box Maze, Abrahams et al., 1997, 1999), and impair performances on virtual reality topographical memory tasks (Spiers et al., 2001b).
More than precise links between particular spatial memory functions and regions within the hippocampal network have been established in some studies. For example, early studies indicated lateralization of hippocampal involvement in memory, with the right medial temporal lobe predominantly associated with visuospatial recall (for instance, Milner, 1965; Smith and Milner, 1981, 1989; Pigott and Milner, 1993; Abrahams et al., 1997; Maguire et al., 1997; Gleissner et al., 1998; Lv et al., 2014), and the left medial temporal lobe with verbal fabric recall (for instance, Saling et al., 1993; Hermann et al., 1997; Martin et al., 2002; Lillywhite et al., 2007). In keeping with this idea, a patient with Pick's illness involving the left temporal lobe showed a complete dissociation between topographical retentivity and verbal retentivity (Maguire and Cipolotti, 1998), although more contempo findings (for instance, Maguire et al., 1996a,b; Grön et al., 2000; Spiers et al., 2001a; Astur et al., 2002; Glikmann-Johnston et al., 2008; Cánovas et al., 2011) support involvement of both the left and correct medial temporal lobes in spatial learning and memory.
The cortices adjacent to the hippocampus, which provide the hippocampus with its main source of direct cortical input and output, accept also been implicated in spatial learning and memory. For instance, some studies indicated bilateral involvement of the parahippocampal gyri (Aguirre et al., 1996, 1998; Aguirre and D'Esposito, 1997; Epstein and Kanwisher, 1998; Mellet et al., 2000; Zeidman et al., 2012), whereas other studies indicate unilateral, predominantly correct-sided involvement (Habib and Sirigu, 1987; Owen et al., 1996; Bohbot et al., 2000; Ploner et al., 2000). In terms of other regions of the hippocampal formation, in non-human primates, cells in the entorhinal cortex are agile during the performance of a variation of the delayed matching to sample chore (memory for objects) and the delayed matching to identify chore (memory for place) (Suzuki et al., 1997). Location-specific activity of neurons has also been recorded within the rat entorhinal cortex (Quirk et al., 1992). Furthermore, lesions to the entorhinal cortex in rats have been shown to result in deficits in acquisition and memory of the Eight-Arm Radial Maze and the Morris Water Maze (Cho and Jaffard, 1995; Nagahara et al., 1995; Davis et al., 2001; Devi et al., 2003). In humans, entorhinal stimulation practical during learning the locations of landmarks enhanced subsequent memory for these locations (Suthana et al., 2012). In a single-neuron recording report, entorhinal cortex neurons activated at multiple related areas of a virtual environs (Miller et al., 2015). Combined lesions of entorhinal and perirhinal cortices dumb rats' performance in spatial memory tasks (Otto et al., 1997; Kaut and Bunsey, 2001). In contrast, perirhinal lesions solitary yielded inconsistent results, with some studies showing impaired operation in certain tests of spatial memory (Wiig and Bilkey, 1994a,b; Liu and Bilkey, 1998a,b,c, 1999, 2001), while in others spatial memory was spared (Glenn and Mumby, 1998; Bussey et al., 1999, 2001; Machin et al., 2002; Ramos, 2002, 2013; Moran and Dalrymple-Alford, 2003). Thus, involvement of the perirhinal cortex in spatial learning and memory may be related to the specific retentivity prototype employed.
In the following section, we provide an overview of 5-HT synthesis, electrophysiology, and receptor distribution to illustrate the concordance between 5-HT receptor distribution and brain areas involved in spatial memory, focusing on the hippocampus (see Figure 1). Subsequently, we review the evidence that 5-HT, mediated by the 5-HT1A receptor, is involved in the modulation of spatial learning and retentivity.
Figure 1. Schematic illustration of brain areas involved in spatial retentivity (
) and the corresponding serotonergic pathways (
) (Adapted from Heimer, 1994, p. 227).
Serotonin (5-Hydroxytryptamine; five-HT) and the 5-HT1A Receptor
Neurons that synthesize 5-HT are clustered in several nuclei along the midline of the brainstem, the most prominent of which are the raphe nuclei. Axons of these neurons innervate most all regions of the central nervous system (CNS) and thus affect a dandy multifariousness of behaviors, such every bit sleep/wake cycle, food intake, sexual behavior, emotional state, and cognitive processes, particularly learning and memory (Frazer and Hensler, 1994). 5-HT is synthesized from the amino acrid tryptophan. The initial stride in synthesis is the conversion of tryptophan to 5-hydroxytryptophan (five-HTP) by the enzyme tryptophan hydroxylase. Aromatic amino acrid decarboxylase (AACD) and then converts five-HTP to 5-HT. 5-HT release occurs via exocytosis and is Ca2+-dependent. After five-HT release, the actions of v-HT in the synapse are terminated past 5-HT transporters, located on the plasma membrane of serotonergic neurons, which reuptake 5-HT back into the serotonergic neurons. v-HT catabolism occurs by monamine oxidase A (MAO-A) (Frazer and Hensler, 1994; Adell et al., 2002).
Seven types of five-HT receptors have been identified, termed 5-HT1-7, and among these are 14 distinct receptor subtypes. Each five-HT receptor subtype has unique structural and pharmacological characteristics and a distinct distribution in the CNS. Of special interest is the 5-HT1A receptor, which is highly concentrated within the hippocampal organization. 5-HT1A receptors are mainly full-bodied in the limbic system, specially the hippocampus (dentate gyrus and CA1), lateral septum, and amygdala, in cingulate and entorhinal cortices, and in the dorsal and median raphe nuclei, many of the regions implicated in spatial learning and memory. In dissimilarity, only low concentrations are present in the striatum, substantia nigra, and the cerebellum (Barnes and Sharp, 1999; Lanfumey and Hamon, 2000). Autoradiography and immunohistochemical methods show that 5-HT1A receptors are located mail-synaptically, also every bit on the serotonergic neurons themselves in the raphe nuclei where they deed equally somatodendritic autoreceptors (Verge et al., 1985, 1986; Hoyer et al., 1986; Pazos et al., 1987; Zifa and Fillon, 1992; Hall et al., 1997; Lanfumey and Hamon, 2000). At the cellular level, 5-HT1A receptors reside on hippocampal pyramidal and granule cells (Lanfumey and Hamon, 2000). The highest density of these receptors are found in the granular layer (Hall et al., 1997).
In both hippocampus and dorsal raphe regions, 5-HT1A receptor activation results in neuronal hyperpolarization through the interaction with G-poly peptide and the opening of Chiliad+ channels (Hamon et al., 1990; Frazer and Hensler, 1994; Lanfumey and Hamon, 2000). Since 5-HT1A receptors are located pre- and post-synaptically, endogenous v-HT and/or v-HT1A receptor agonists have different effects. 5-HT1A somatodentritic autoreceptors modulate synaptic manual. When activated via endogenous 5-HT and/or five-HT1A receptor agonists, they inhibit the serotonergic neuron on which they reside, and reduce 5-HT release. In contrast, at post-synaptic receptors such as occur in the hippocampus, v-HT1A agonists facilitate 5-HT neurotransmission (Lanfumey and Hamon, 2000). Encephalon areas that are disquisitional for spatial learning and memory, such equally those that are office of the hippocampal formation, harbor the post-synaptic 5-HT1A receptors.
v-HT1A and Spatial Learning and Retentiveness
Evidence to support a role for the five-HT1A receptor in spatial learning and retentiveness comes from a diversity of experimental methods, including mouse "knockout" models, direct receptor activation and blockade, neurotransmitter PET imaging, genetic studies, and manipulation of v-HT concentrations. We organize this review according to the primary experimental method used. Studies cited hither are summarized in Table i.
Tabular array i. Summary of the studies cited according to the experimental method used.
Knockout Mouse Models
Studies using genetically modified animals, particularly those of unmarried gene deletions in knockout mice, provide the strongest bear witness for the role of the v-HT1A receptor in learning and memory (encounter Bert et al., 2008 for a review of learning and memory in 5-HT1A-receptor mutant mice). Sarnyai et al. (2000) assessed 5-HT1A-scarce mice on hippocampal-related spatial learning and retentivity tasks, the Morris Water Maze and the "Y" shape Maze. Their results showed that lack of five-HT1A receptors is specifically associated with spatial learning and memory impairments. Wolff et al. (2004) demonstrated like impairments in learning and retention of the Morris Water Maze in immature-adult five-HT1A knockout mice, merely not in aged five-HT1A knockout mice. The authors suggested that the reduced effect of the mutation in aged animals maybe reflects the lower efficacy of autoreceptors due to crumbling and/or a prevalence of hippocampal heteroreceptors.
5-HT1A Receptor Stimulation
five-HT1A agonists and antagonists modulate 5-HT neurotransmission and have been shown to directly alter spatial learning performance. Typically, antagonists have been constitute to impair spatial retentiveness, whereas agonists are institute to ameliorate the antagonist-induced spatial deficits, or allowed normal functioning. For example, in a report by Micheau and Van Marrewijk (1999), intra-peritoneal administration of the 5-HT1A receptor agonist viii-hydroxy-2-(di-n-propylamino) tetraline (8-OH-DPAT) improved conquering of a spatial discrimination task in an 8-arm radial maze. An intra-septal infusion of 8-OH-DPAT produced the same pattern of findings, although the improvement was less pronounced. Bertrand et al. (2000) showed contradictory findings, however, reporting that intra-septal infusion of viii-OH-DPAT impaired spatial learning. Administration of eight-OH-DPAT into the rat dorsal raphe had no upshot on Delayed Non-Matching to Position (spatial working retentivity) chore functioning at any dose. In comparison, administration of the same compound into the median raphe improved performance accuracy. When 8-OH-DPAT was administered into the dorsal hippocampus, however, information technology produced a small-scale impairment in performance (Warburton et al., 1997). 8-OH-DPAT also impaired performance on a h2o maze task (Carli et al., 1995) and on the viii-arm radial maze (Egashira et al., 2006). These findings demonstrate dissimilar outcome for pre- and post-synaptic 5-HT1A receptor stimulation on spatial learning and memory tasks.
Additional evidence for the part of five-HT1A receptor agonists in spatial memory comes from animal models of traumatic brain injury (TBI). In this model, animals are subjected to controlled cortical lesion to mimic TBI, and then retention is examined at different fourth dimension points following injury and after assistants of five-HT1A agonists. These studies showed that TBI-induced spatial memory deficits are attenuated by handling with the 5-HT1A receptor agonist buspirone (Olsen et al., 2012) and 8-OH-DPAT (Cheng et al., 2008). Furthermore, a combined therapeutic regimen of buspirone and environmental enrichment was establish to be more effective than either lone in enhancing spatial learning in brain injured pediatric rats (Monaco et al., 2014).
Imaging Serotonergic Neurotransmission
Because the 5-HT1A receptor plays an important role in a range of physiological processes and in the pathophysiology of a variety of psychiatric and neurodegenerative disorders, synthesis of 5-HT1A receptor agents has been carried out primarily for their therapeutic potential. In contempo years, more than 20 compounds take been labeled with carbon-11, fluorine-18, or iodine-123 for imaging and quantification of the 5-HT1A receptor with PET and SPECT (for review meet Passchier and Van Waarde, 2001). The almost successful radioligands thus far are [carbonyl-11C] WAY-100635 (WAY), [carbonyl-elevenC]desmethyl-Style 100635 (DWAY), 2′-methoxyphenyl-(N-2′-pyridinyl)-p-[xviiiF]fluoro-benzamidoethylpiperazine ([18F]MPPF), and [xiC]robalzotan (NAD-299) (Passchier and Van Waarde, 2001). To the best of our knowledge, the only written report that examined 5-HT1A receptor density and spatial learning and memory (i.e., object-location, navigation, and floor program drawing) in humans using the PET ligand [18F]MPPF was recently published by our group (Glikmann-Johnston et al., 2015). In this report, healthy participants performed spatial virtual environment tasks during PET scanning. We institute an association betwixt hippocampal asymmetry in [18F]MPPF binding and performance on the object-location task. A lower binding potential in the correct vs. the left hippocampus was related to better memory operation. This finding indicates that reduced right vs. left hippocampal 5-HT1A receptor availability enhances object-place associative memory. Although not inside the scope of this review, information technology is important to notation that Theodore et al. (2012) used similar experimental methodology in verbal retentiveness using the 18FCWAY PET ligand. In their study, reduced left hippocampal 5-HT1A receptor binding in temporal lobe epilepsy (TLE) patients was related to delayed auditory verbal memory impairment, contained of the side of the epileptic focus. More cognitive serotonergic imaging studies are needed to build up the evidence for the office of 5-HT1A receptor in fundamental components of human spatial memory.
Genetic Variance in five-HT1A Receptor Availability
Congenital differences in 5-HT1A receptor availability were constitute to be related to spatial memory, specifically length variations in the serotonin-transporter-gene-linked polymorphic region (5-HTTLPR). 5-HTTLPR is a 44-base of operations pair insertion/deletion functional polymorphism in the promotor region of the serotonin transporter (5-HTT) gene (Lesch et al., 1996). This polymorphism produces two mutual alleles designated long (L) and short (S), and was found to bear upon 5-HT1A receptor availability (David et al., 2005). Man (Roiser et al., 2006, 2007) and primate (Jedema et al., 2010) carriers of S allele demonstrated superior performance compared to L carriers on a diverseness of cognitive tasks, including hippocampal-dependent visual retentivity tasks (a computerized version of the Cake Blueprint subtest of the Wechsler Adult Intelligence Examination and the CANTAB Pattern Recognition Retentiveness and Delayed Match to Sample).
Manipulations of 5-HT Levels
Pharmacological alterations of 5-HT concentrations, past altering either five-HT release or reuptake, accept been shown to influence spatial memory. Overall, increased extracellular 5-HT concentrations maintain or improve memory operation, and reduced levels of the neurotransmitter impair spatial memory. Changes in five-HT release are thought to indirectly stimulate mail service-synaptic v-HT1A receptors, which reside on areas important to spatial learning and memory, thereby affecting retentiveness function (Lesch et al., 1996; Kuypers and Ramaekers, 2005). Support for this hypothesis is plant in a study by du Jardin et al. (2014) with the utilize of parachlorophenylalanine (PCPA). This compound inhibits tryptophan hydroxylase, and thus reduces 5-HT synthesis. In their study, PCPA induced v-HT depletion in rats and caused retentiveness deficits on object recognition and Y-maze spontaneous alternation tests. The selective 5-HT1A receptor agonist flesinoxan significantly occupied v-HT1A receptors and restored PCPA-induced memory deficits in both tests. Although other agents had similar effects on spatial retentiveness part (e.thousand., 3,iv-methylenedioxymethamphetamine/MDMA : Play a trick on et al., 2000; Skelton et al., 2006; Vorhees et al., 2007; Fisk et al., 2011; D-fenfluramine : Morford et al., 2002; methamphetamine : Vorhees et al., 1994, 2000, 2008; Schröder et al., 2003), studies to date did non involve the 5-HT1A receptor directly. Even though the v-HT1A receptor is the most abundant in the hippocampus, it is not possible to exclude other receptor subtypes that v-HT stimulate in this expanse (5-HT2A, 5-HT6, and 5-HT7), and that may accept an effect on spatial memory.
Determination
The findings reviewed here provide converging evidence in support of the hypothesis that 5-HT, mediated by the v-HT1A receptor, plays a primal role in hippocampal-dependent spatial memory in animals and humans. Stiff bear witness comes from knockout mouse models. These studies accept shown that v-HT1A receptor knockouts are specifically associated with deficits in performance on spatial retentivity tasks. A diversity of agonists and antagonists active at the 5-HT1A receptor attune v-HT neurotransmission and induce a alter in spatial learning. Blockade of the 5-HT1A receptor impairs spatial memory, while receptor activation ameliorates antagonist-induced spatial retention deficits. Another line of show emerges from studies that vary neurotransmitter levels pharmacologically. Typically, increased five-HT extracellular concentrations maintain or improve memory operation, and reduction in neurotransmitter levels impairs spatial retention.
Recent advances in human neurotransmitter research methods permit for more directly quantification of 5-HT1A receptor availability during spatial learning and retentiveness. Initial results from neuroimaging studies with the utilize of neurotransmitter PET signal the contribution of endogenous serotonin release or 5-HT1A receptor density to spatial retentiveness, particularly to the ability to recall the location of objects in the surround (Glikmann-Johnston et al., 2015). The mapping of the human genome provides further evidence at the individual person level for the association betwixt five-HT1A receptor density and spatial memory.
Theories of hippocampal involvement in spatial memory include: (a) the cognitive map theory of O'Keefe and Nadel (1978); (b) the theory proposed past Olton and colleagues (Olton et al., 1979; Olton and Paras, 1979), in which the hippocampus is crucial for working memory; and, (c) the theory that attributes a binding mechanism to the hippocampus to form spatial memories such as object location (for example, Chalfonte et al., 1996; Eichenbaum et al., 1996). The evidence reviewed in this paper involving 5-HT, peculiarly the 1A receptor subtype, and spatial memory is further supported past the well-established notion of the interest of the hippocampus in spatial retention function.
A substantial number of studies accept examined the role of 5-HT in spatial learning and memory and have demonstrated, particularly in animals, a stiff relation between five-HT and spatial memory. Yet several pregnant questions remain. We suggest that boosted research is needed to clarify the relationship between 5-HT1A receptor modulation and specific aspects of spatial memory, including object location and spatial frames of reference, allocentric vs. egoistic representations, and navigation and episodic retention inside a topographical framework (Burgess et al., 2002; Burgess, 2008). Also, research is needed into how the serotonergic system interacts with other major neurotransmitter systems, including the acetylcholineric system, to modulate spatial memory.
For patients with damage to the temporal lobes due to progressive pathology such as Alzheimer's disease, impairments of spatial retentiveness are often the first symptoms reported. The idea that hippocampal 5-HT1A receptor plays a primal role in spatial learning and memory may exist informative for early intervention strategies, and for improving patient outcomes in diseases affecting the temporal lobes.
Author Contributions
YG-J, MS, DR, and JS wrote the commodity, reviewed the article, and approved the last version for publication.
Conflict of Interest Argument
The authors declare that the research was conducted in the absenteeism of any commercial or fiscal relationships that could be construed as a potential conflict of involvement.
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Damage To Which Of The Following Brain Areas Disrupts Spatial Learning?,
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