Anxiolytic-like effects of substance P administration into the dorsal, but not ventral, hippocampus and its influence on serotonin

Carvalho, Milene Cristina de; Masson, Sueli; Brandão, Marcus Lira; Silva, M.A. de Souza

doi:10.1016/j.peptides.2008.02.014

Cited by 23 publications

(17 citation statements)

References 74 publications

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“…Alternatively, this effect may be related to an altered emotional reaction to the task rather than to impaired motor capabilities. Such a possibility is in agreement with a role for the hippocampus, including its dorsal part, in controlling anxiety behaviors (Gray, 1982;Gray and McNaughton, 2003;Carvalho et al, 2008). Given that recent evidence showed that sst has anxiolytic-like effects and suppresses the frequency of hippocampal theta rhythm induced by reticular stimulation, a neurophysiological signature common to all classes of anxiolytic drugs (Engin et al, 2008), sst 2 agonists may have reduced motivation to solve the water maze task that is based on water aversion.…”

Section: Discussionsupporting

confidence: 66%

Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: Functional relevance in interactive memory systems

et al. 2009

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The hippocampal somatostatin (sst) receptor subtype 4 (sst(4)) modulates memory formation by diminishing hippocampus-based spatial function while enhancing striatum-dependent behaviors. sst(4)-mediated regulations on neuronal activity in the hippocampus appear to depend on both competitive and cooperative interactions with sst receptor subtype 2 (sst(2)). Here, we investigated whether interactions with sst(2) receptors are required for sst(4)-mediated effects on hippocampus-dependent spatial memory and striatum-dependent cued memory in a water maze paradigm. Competition was assessed in mice by intrahippocampal injections of the sst(4) agonist L-803,087 alone or combined with sst(2) agonists (L-779,976 or octreotide). Effects of L-803,087 were also tested in sst(2) knockout mice to assess for receptor cooperation. Finally, sst(2a) and sst(4) localizations within hippocampal subregions were analyzed by immunohistochemistry and expression levels of sst(2a) and sst(2b) were quantified by real-time qPCR. Hippocampal injections of L-803,087 impaired spatial memory but enhanced cued memory. The latter effect was lost not only in sst(2) knockout mice but also in the presence of sst(2) agonists, whereas the former effect remained unaffected by sst(2) agonists or gene deletion. Octreotide and L-779,976 did not yield memory effects but reduced swim velocity throughout the acquisition trials suggesting that stimulation of sst(2) affected motivation and/or anxiety. sst(2a) and sst(4) were respectively detected in the dentate gyrus (DG) and the CA1 subfield suggesting that their functional interactions are not mediated by direct receptor coupling. Hippocampus sst(2a) expression was 36-fold higher than sst(2b). Possible neural mechanisms and functional significances for interaction between memory systems in relationship with stress-induced changes in hippocampal functions are discussed.

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Section: Discussionsupporting

confidence: 66%

Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: Functional relevance in interactive memory systems

et al. 2009

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“…Kertes et al [27] recently showed that SP facilitates passive avoidance learning when injected either into the GP or into the amygdaloid (AMY) body, and also showed that SP and NK1Rs play important roles in pallidal positive reinforcing mechanisms [28]. In agreement with these studies, SP infused into the ventral hippocampus (VH) but not dorsal hippocampus (DH) had an effect on both mnemonic and emotional processes [2]. SP can have neurotrophic as well as memory-promoting effects upon direct application into the region of the nucleus basalis magnocellularis (NBM) [29].…”

Section: Discussionmentioning

confidence: 76%

“…The neuropeptide substance P (SP) and its high affinity receptor neurokinin 1 receptor (NK1R) in the central nervous system are known to be involved in several processes such as inflammation, blood pressure, motor behavior, anxiety, and learning and memory [1,2] Many studies have shown that the neurokinin SP can have memory-promoting, reinforcing and anxiolytic-like effects when administered systemically or into the nucleus basalis of the ventral pallidum and that SP and certain SP-fragments may be considered to have beneficial behavioral effects in normal animals [3]. SP has excitatory effects in the hippocampus and is able to facilitate long term potentiation (LTP) via activation of NK1R in the hippocampus [4].…”

Section: Introductionmentioning

confidence: 99%

The Role of Substance P in the Marginal Division of the Neostriatum in Learning and Memory is Mediated Through the Neurokinin 1 Receptor in Rats

et al. 2011

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Substance P (SP) is a neuropeptide that plays an important role in inflammation, respiration, pain, aggression, anxiety, and learning and memory mainly through its high affinity neurokinin 1 receptor (NK1R). The marginal division (MrD) is a pan-shaped subdivision in the caudomedial margin of the neostriatum in the mammalian brain and is known to be involved in learning and memory. We studied the expression of SP, NK1R and NK1R mRNA in the rat striatum by immunohistochemistry, immunofluorescence and in situ hybridization, and found that the levels of SP, NK1R protein and NK1R mRNA were high in the cell bodies, fibers and terminals of neurons in the neostriatum, especially in the MrD. Knocking down NK1R activity in the MrD by using an antisense oligonucleotide against NK1R mRNA inhibited learning and memory in a Y-maze behavioral test. Our results show that NK1R mediates the role of SP in the MrD in learning and memory.

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“…2c). This may explain the inconsistent findings in rodent fear conditioning studies following lesions or inactivation of either dorsal or ventral hippocampus 29,[104][105][106] (in which some studies find effects of dorsal not ventral lesions, and vice versa). That is, the effects on conditioned fear may be a function of the locus of the hippocampal lesion with respect to the dorsoventral hippocampus to mediolateral amygdala topography.…”

Section: Emotionmentioning

confidence: 99%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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The precise functional role of the hippocampus remains a topic of much debate. According to a dominant view, the dorsal/posterior hippocampus is implicated in memory and spatial navigation and the ventral/anterior hippocampus mediates anxietyrelated behaviours. However, this 'dichotomy view' may need revision. Gene expression studies demonstrate multiple functional domains along the hippocampal long axis, which often exhibit sharply demarcated borders. By contrast, anatomical studies and electrophysiological recordings in rodents suggest that the long-axis is organized along a gradient. Together, these observations suggest a model in which functional long-axis gradients are superimposed on discrete functional domains. This model provides a potential framework to explain and test the multiple functions ascribed to the hippocampus.The hippocampus is a medial temporal lobe structure critically involved in episodic memory and spatial navigation [1][2][3][4][5][6][7] . Its long, curved form is present across all mammalian orders and runs along a dorsal (septal) to ventral (temporal) axis in rodents, corresponding to a posteriorto-anterior axis in humans (FIG. 1a-b). The same basic intrinsic circuitry is maintained throughout the long axis and across species (FIG. 1c). Despite this conserved intrinsic circuitry, the dorsal and ventral portions have different connectivities with cortical and subcortical areas, and this has long posed a question as to whether the hippocampus is functionally uniform along this axis. Here we review cross-species data that show how the seemingly disparate functions ascribed to the hippocampus can be accommodated by a model in which different functional properties exist along the longitudinal axis.The severe memory impairment suffered by patient H.M. following bilateral hippocampal resection 1 led to intensive study 8 of patients and animal models with hippocampal damage, with an ensuing characterisation of hippocampal function in terms of declarative memory 2 , encompassing both episodic and semantic memory. At the same time, however, evidence emerged for a hippocampal role in spatial memory, based on the discovery of hippocampal 'place cells' 9,10 and the demonstration that hippocampal lesions impair spatial memory 4 . Both the declarative memory hypothesis 11 and the spatial mapping hypothesis 12 of hippocampal function proposed a unitary model in which the entire hippocampus is dedicated

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Anxiolytic-like effects of substance P administration into the dorsal, but not ventral, hippocampus and its influence on serotonin

Cited by 23 publications

References 74 publications

Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: Functional relevance in interactive memory systems

Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: Functional relevance in interactive memory systems

The Role of Substance P in the Marginal Division of the Neostriatum in Learning and Memory is Mediated Through the Neurokinin 1 Receptor in Rats

Functional organization of the hippocampal longitudinal axis

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