Anxiety is functionally segregated within the septo-hippocampal system
Abstract
Previous lesion studies have suggested that the septal-hippocampal system is involved in fear and anxiety. In this study we examined the effects on anxiety of temporary neuronal inhibition of various aspects of the septo-hippocampal system in rats. Infusions of tetrodotoxin (TTX) were used to induce reversible lesions in the fimbria fornix, medial septum, dorsal hippocampus, and ventral hippocampus. To assess anxiety we used the elevated plus-maze and the shock-probe burying tests. A reduction in anxiety in the elevated plus-maze is indicated by increased open arm exploration, whereas a reduction in anxiety in the shock-probe burying test is indicated by decreased burying behavior or increased contacts with the shock-probe. The results suggested that inhibition of the septal-hippocampal system induced site-specific anxiolytic effects that vary in nature. Tetrodotoxin lesions of the fimbria fornix increased both open arm exploration and the number of shocks taken by the rats, while having no effect on burying behavior. Both septal and ventral hippocampal lesions increased open arm exploration and decreased burying behavior, but had no effect on the number of probe shocks. Finally, TTX lesions of the dorsal hippocampus increased the number of shocks taken by the rats, but did not affect open arm activity or burying behavior. Neuroanatomical studies indicated that the effect on the number of shocks induced by dorsal hippocampal TTX lesions was not likely mediated by the amygdala. Collectively, the data suggest that the control of specific anxiety reactions is functionally segregated within different aspects of the septo-hippocampal system.
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The neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients.
“This contrast notwithstanding, the neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients26-34, underscoring the utility and translatability of these rodent studies.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [27]
Glutamatergic terminals of BLA fibers onto pyramidal neurons in the CA1 region of the vHPC bidirectionally control innate anxiety-related behaviors in the EPM and OFT, such that increased activity in this projection enhances anxiety-like behavior and inactivation reduces anxiety-like behavior.
“Furthermore, glutamatergic terminals of BLA fibers onto pyramidal neurons in the CA1 region of the vHPC bidirectionally control innate anxiety-related behaviors in the EPM and OFT66, such that increased activity in this projection enhances anxiety-like behavior and inactivation of this pathway reduces anxiety-like behavior27,66.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [27]
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Resolving the neural circuits of anxiety
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“…well established technique used to examine the involvement of the vHipp in numerous behavioral (Ambrogi Lorenzini et al., 1997; Zhang et al., 2002; Degroot and Treit, 2004), neurochemical (Legault and Wise, 1999; Peterschmitt et al., 2005), and electrophysiological (Floresco et al., 2001) studies.”
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“Anxiety, depression, dissociation, and temporal lobe epilepsy-like symptoms have all been associated with aspects of hippocampal function (12, 25– 29).”
BackgroundDistributed circuits underlying anxiety
Adhikari, A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00112 · Cited by 204 · see citing works
To Approach or Avoid: An Introductory Overview of the Study of Anxiety Using Rodent Assays
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“When inactivated, the medial septum increases the time spent in the EPM open arms (Degroot and Treit, 2004).”
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“The anxiety tasks used have been shown to be modulated in part by the hippocampus (Degroot and Treit, 2004; Wartella et al., 2003), however, other studies have indicated that the amygdala may modulate anxiety behaviors in these tasks (Mchugh et al.”
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“…of important functional differences between dorsal and ventral regions of the hippocampus, the first being closely related to learning/memory processes while the latter would be more involved in anxiety (Kjelstrup et al. 2002; Bannerman et al. 2004; Degroot and Treit 2004; Bertoglio et al. 2006).”
BackgroundResultFurther evidence that anxiety and memory are regionally dissociated within the hippocampus
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“In contrast, the ventral hippocampus (VH) has been associated with regulation of anxiety and is assumed to exert its effects mainly through connections with the amygdala and hypothalamus (Kjelstrup et al., 2002; Bannerman et al., 2003, 2004; Degroot and Treit, 2004; Trivedi and Coover, 2004).”
BackgroundLateral septum as a nexus for mood, motivation, and movement
Wirtshafter, H. S., & Wilson, M. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.029 · Cited by 122 · see citing works
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“This suggestion was originally based on the observation that the behavioral effects of anxiolytics parallel those of either permanent or temporary lesions to the septum and/or the hippocampus (Gray and McNaughton 2000; Degroot and Treit 2004).”
BackgroundUnique regulation of long term potentiation in the rat ventral hippocampus
Maggio, N., & Segal, M. (2007) · Hippocampus · doi:10.1002/hipo.20237 · Cited by 100 · see citing works
“Later studies also demonstrated that the ventral hippocampus, more than the dorsal one, is involved in the development of affective disorders (Kjelstrup et al., 2002; Degroot and Treit, 2004).”
ResultNeurogenesis and antidepressant action
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“The role of the fornix is best established within the domain of episodic memory (Rolls, 2015); its contribution to the processing of emotion is more controversial and has been more widely studied in animal models (Decker et al., 1995; Degroot and Treit, 2004; Acevedo et al., 2012).”
BackgroundEadie, B. D., Zhang, W. N., Boehme, F., Gil‐Mohapel, J., Kainer, L., Simpson, J. M., & Christie, B. R. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.08.001 · Cited by 94 · see citing works
“The ventral hippocampus is a brain region strongly linked to anxiety-related behaviors (Bannerman et al., 2004, 1999; Degroot and Treit, 2004; Engin and Treit, 2007), while the dorsal hippocampus appears to be subservient to spatial learning and memory (Engin and Treit, 2007; Maurer et al., 2005;…”
BackgroundDifferential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning
Esclassan, F., Coutureau, É., Scala, G. D., & Marchand, A. R. (2008) · Hippocampus · doi:10.1002/hipo.20473 · Cited by 92 · see citing works
“It has thus been suggested that this region plays a general role in the expression of anxietyrelated behaviors (Richmond et al., 1999; Bannerman et al., 2004; Degroot and Treit, 2004; McHugh et al., 2004).”
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“infusion of GABAA receptor agonists—direct or indirect— reduced anxiety-like behavior in the plus-maze, a finding which is also consistent with the effects of electrolytic, excitotoxic, or temporary TTX lesions of the septum (Pizzo et al., 2002; Menard and Treit, 1996; Pesold and Treit, 1994; Degroot et al., 2001; Deg…”
InfluentialSelf-citationA role for the extracellular signal-regulated kinase signal pathway in depressive-like behavior
Qi, X., Lin, W., Wang, D., Pan, Y., Wang, W., & Sun, M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.051 · Cited by 84 · see citing works
“Previous esion studies indicate that some brain region may play an espeially important role in some specific behavior, and disruption of he different brain areas may produce different behavioral disorers [8,19,27].”
Backgroundα-Synuclein transgenic mice exhibit reduced anxiety-like behaviour
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Dissecting the Fornix in Basic Memory Processes and Neuropsychiatric Disease: A Review
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“It has been hypothesized that the fornix plays an important role in the mediation of fear and anxiety (Degroot and Treit, 2004) as well as daily stress, as the conduit of glucocorticoids to the hippocampus (Savransky et al.”
Altered fimbria-fornix white matter integrity in anorexia nervosa predicts harm avoidance
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“However, since fimbria-fornix FA predicted Harm Avoidance bilaterally and that region has been repeatedly associated with anxiety modulation (Degroot and Treit, 2004; Duarte et al., 2010), we believe that this finding is not simply by chance.”
Hippocampal dysfunction and cognitive impairment in Fragile-X Syndrome
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“Several lines of evidence suggest that while the dorsal hippocampus is mainly involved in spatial learning and memory, the ventral region of this structure plays a more prominent role in mood and affective behaviors (Bannerman et al., 2004, Degroot and Treit, 2004, Engin and Treit, 2007).”
BackgroundEngin, E., & Treit, D. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282d28f6f · Cited by 78 · see citing works
“The shock-probe burying data most often violate assumptions of normality and homogeneity of variance (e.g. Degroot and Treit, 2004).”
BackgroundSelf-citationHale, M. W., Hay-Schmidt, A., Mikkelsen, J. D., Poulsen, B. C., Shekhar, A., & Lowry, C. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.054 · Cited by 77 · see citing works
Trent, N. L., & Menard, J. L. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.04.035 · Cited by 76 · see citing works
The Avian Hippocampal Formation and the Stress Response
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“Lesions of the temporal (but not the septal) hippocampus also have an anxiolytic effect [McHugh et al., 2004], although it depends on how anxiety is measured [Degroot and Treit, 2004].”
Adult neurogenesis: Optimizing hippocampal function to suit the environment
Glasper, E. R., Schoenfeld, T. J., & Gould, E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.013 · Cited by 73 · see citing works
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“2005) while lesions of the vHIPP have anxiolytic effects (Bannerman et al. 2003; Degroot and Treit 2004), we hypothesize that the reduced emotionality observed in FAAH null mice might mostly depend on their higher 5-HT-ergic tone in FC.”
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“…2002; Burns et al. 1996; McHugh et al. 2004), exposure to predator-related stimuli (Blanchard et al. 2005; Pentkowski et al. 2006), elevated plus maze (Degroot and Treit 2004; Kjelstrup et al. 2002; Trivedi and Coover 2004) and tone fear conditioning (Hunsaker and Kesner 2008; Maren and Holt 2004).”
BackgroundAdams, W. K., Kusljic, S., & van den Buuse, M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.035 · Cited by 74 · see citing works
The Medial Septum as a Potential Target for Treating Brain Disorders Associated With Oscillopathies
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“Pharmacological inhibition of the MS (with tetrodotoxin, muscimol, or lidocaine infusion) decreased unconditioned and conditioned anxiety (Degroot et al., 2001; Degroot and Treit, 2004; Lamprea et al., 2010), whereas pharmacological activation of the MS (with bicuculline) increased anxiety in rats (Ashabi et al.”
BackgroundAujla, H., Martin‐Fardon, R., & Weiss, F. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301588 · Cited by 69 · see citing works
“The septum is a structure that is known to play an important role in the regulation of defensive burying (Menard and Treit, 2001; Degroot and Treit, 2003, 2004) and that may show changes in glutamatergic function that contribute to the differential sensitivity to the effects of LY379268 on…”
BackgroundChandna, A. R., Kuhlmann, N., Bryce, C. A., Greba, Q., Campanucci, V. A., & Howland, J. G. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.063 · Cited by 68 · see citing works
“Increased open arm time in the elevated plus maze has also been noted following inactivation of either the hippocampus (Degroot and Treit, 2004) or medial prefrontal cortex (Shah et al., 2004).”
The serotonin 1A receptor gene as a genetic and prenatal maternal environmental factor in anxiety
Gleason, G., Liu, B., Bruening, S., Zupan, B., Auerbach, A. D., Mark, W. H., Oh, J.-E., Toth, J. G., Lee, F., & Tóth, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914805107 · Cited by 62 · see citing works
“Because gestational stress, in addition to inducing permanent emotional deficits (13), also affects the development of the DG (14, 15), among other brain regions, we focused on the hippocampus, in particular on its ventral subdivision implicated in anxiety (9, 16, 17).”
BackgroundEffects of pair-housing after social defeat experience on elevated plus-maze behavior in rats
Nakayasu, T., & Ishii, K. (2008) · Behavioural Processes · doi:10.1016/j.beproc.2008.02.007 · Cited by 61 · see citing works
“An increase in time spent in he open arms is the conventional index of anxiety reduction e.g., Degroot and Treit, 2004; Pellow et al., 1985; Rodgers and ohnson, 1995).”
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“For example, the septum and amygdala send axons to the hippocampus, and both of these structures are distinctively involved in fear processing (e.g., Corcoran et al., 2005; Degroot and Treit, 2004; Pesold and Treit, 1994).”
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Irisin Acts via the PGC-1α and BDNF Pathway to Improve Depression-like Behavior
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“Depression is associated with damage in several regions of the brain such as the hippocampus, and linked to mood dysregulation, increased anxiety, fatigue, reduced attention, reduced self-esteem, disturbed sleep pattern, and hopeless behavior pattern [4,5].”
BackgroundMineur, Y. S., Mose, T. N., Vanopdenbosch, L., Etherington, I. M., Ogbejesi, C., Islam, A., Pineda, C. M., Crouse, R. B., Zhou, W., Thompson, D. C., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01404-7 · Cited by 48 · see citing works
Modulation of anxiety by μ-opioid receptors of the lateral septal region in mice
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“, the anterior hippocampus in primates) appears to be mainly implicated in the regulation of stress responses, emotions, and affect (Bannerman et al., 2004; Degroot and Treit, 2004).”
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“Functional distinctions in the hippocampus generally align with anatomical distinctions: the ventral hippocampus is generally more involved in stress, anxiety, and fear and the dorsal hippocampus generally more involved in spatial memory (Degroot and Treit, 2004; Hunsaker and Kesner, 2008; Kjelstrup et al., 2002; Mare…”
BackgroundLiberto, V. D., Frinchi, M., Verdi, V., Vitale, A., Plescia, F., Cannizzaro, C., Massenti, M. F., Belluardo, N., & Mudò, G. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4498-0 · Cited by 41 · see citing works
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“…in the ventral hippocampus of the rat since this hippocampal region is most often associated with affective states (McHugh et al., 2004; Degroot and Treit, 2004; Kjelstrup et al., 2002; Bannerman et al., 2003) and second, to determine whether GRs mediate corticosterone-stimulated 5-HT…”
BackgroundWorkman, J. L., Chan, M. Y. T., & Galea, L. A. M. (2014) · Hippocampus · doi:10.1002/hipo.22375 · Cited by 39 · see citing works
“Indeed, the ventral hippocampus is preferentially involved in stress, anxiety, and fear (Kjelstrup et al., 2002; Degroot and Treit, 2004; Maren and Holt, 2004; Trivedi and Coover, 2004; Hunsaker and Kesner, 2008) compared with the dorsal hippocampus.”
BackgroundSchwerdtfeger, R. M. H., & Menard, J. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.011 · Cited by 39 · see citing works
The role of the dorsal and ventral hippocampus in fear and memory of a shock-probe experience
McEown, K., & Treit, D. (2008) · Brain Research · doi:10.1016/j.brainres.2008.11.041 · Cited by 39 · see citing works
Self-citationA novel role of circadian transcription factor DBP in hippocampal plasticity
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Intrahippocampal Anisomycin Impairs Spatial Performance on the Morris Water Maze
Dubue, J. D., McKinney, T. L., Treit, D., & Dickson, C. T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1857-15.2015 · Cited by 36 · see citing works
“These behavioral deficits were similar to those previously observed following direct suppression of the hippocampus using sodium channel blockers such as TTX and GABAA receptor agonists such as muscimol (Degroot and Treit, 2004; McEown and Treit, 2010).”
ResultInfluentialSelf-citationInhibiting medial septal cholinergic neurons with DREADD alleviated anxiety-like behaviors in mice
Zhang, Y., Jiang, Y., Shao, S. H., Zhang, C., Liu, F., Wan, Y., & Yi, M. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.12.010 · Cited by 37 · see citing works
Serotonin and the Neurobiology of Anxious States
Lowry, C. A., & Hale, M. W. (2010) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(10)70091-6 · Cited by 36 · see citing works
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“For example, temporary inactivation of the medial septum produced a significant increase in the percent of time spent on the open arms of the elevated plus maze ( Degroot and Treit 2004 ).”
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“…and owan, 1977; Witter et al., 1989), and its ventral part is mplicated in stress integration through its connections to he hypothalamo-pituitary-adrenocortical axis (Kjelstrup et l., 2002; Bannerman et al., 2003; Degroot and Treit, 2004; ortical areas (A, B), the dorsal hippocampal formation (C–”
Yeung, M., Engin, E., & Treit, D. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2248-x · Cited by 34 · see citing works
Self-citationPentkowski, N. S., Litvin, Y., Blanchard, D. C., Vasconcellos, A., King, L. B., & Blanchard, R. J. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.02.007 · Cited by 34 · see citing works
“…anxiolytic-like effects in the shock-probe burying, social interaction, light/dark and hyponeophagia tests of defense (Bannerman et al., 2003; Degroot & Treit, 2004; McHugh et al., 2004), with these results resembling the anxiolytic-like effects induced by benzodiazepines in many of the same…”
BackgroundResultInfluentialIs full physical contact necessary for buffering effects of pair housing on social stress in rats?
Nakayasu, T., & Kato, K. (2010) · Behavioural Processes · doi:10.1016/j.beproc.2010.12.002 · Cited by 34 · see citing works
Anxiolytic-like effect of group III mGlu receptor antagonist is serotonin-dependent
Stachowicz, K., Chojnacka-Wójcik, E., Kłak, K., & Pilc, A. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.08.002 · Cited by 33 · see citing works
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“Besides reducing buryingbehavior [57], it has been shown that hippocampal lesions increase open arm and central area permanence in the EPM and OFT, respectively [58].”
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Self-citationMoreno, E., Vaz, S. H., Cai, N.-S., Ferrada, C., Quiroz, C., Barodia, S. K., Kabbani, N., Canela, E. I., McCormick, P. J., Lluı́s, C., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0191-11.2011 · Cited by 31 · see citing works
“Interestingly, injection of acetylcholine into the ventral, but not the dorsal, hippocampus, reduces anxiety (Degroot and Treit, 2004).”
Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal
Turner, J. R., Wilkinson, D. S., Poole, R. L., Gould, T. J., Carlson, G. C., & Blendy, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.105 · Cited by 29 · see citing works
Fluoxetine Disrupts the Integration of Anxiety and Aversive Memories
Degroot, A., & Nomikos, G. G. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300624 · Cited by 30 · see citing works
“For instance, both electrolytic and excitoxic lesions of the hippocampus induce anxiolysis and impair learning and memory (Degroot and Treit, 2004; Fanselow, 2000; Treit and Menard, 1997).”
BackgroundSelf-citationThe HDAC Inhibitor Phenylbutyrate Reverses Effects of Neonatal Ventral Hippocampal Lesion in Rats
Sandner, G., Host, L., Angst, M.-J., Guiberteau, T., Guignard, B., & Zwiller, J. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2010.00153 · Cited by 29 · see citing works
Petrides, T., Georgopoulos, P., Kostopoulos, G., & Papatheodoropoulos, C. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0681-6 · Cited by 29 · see citing works
“fear conditioning (Burman et al. 2006; Hobin and Maren 2006; Kjelstrup et al. 2002; Richmond et al. 1999; Rudy and Matus-Amat 2005; SteVenach et al. 2005; Trivedi and Coover 2006) and anxiety (Bannerman et al. 2004; Degroot and Treit 2002, 2004; Kjelstrup et al. 2002; Pentkowski et al. 2006) are segregated along the d…”
BackgroundInvolvement of the CA1 GABAA receptors in MK-801-induced anxiolytic-like effects
Naseri, M. H., Tackallou, S. H., Nami, M., Zarrindast, M., & Nasehi, M. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000037 · Cited by 28 · see citing works
“This hypothesis was originally based on the anxiolytic effects observed following either permanent or temporary lesions in the septum or the hippocampus (McNaughton and Gray, 2000; Degroot and Treit, 2004).”
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Stachowicz, K., Kłak, K., Pilc, A., & Chojnacka-Wójcik, E. (2005) · PubMed · Cited by 27 · see citing works
Anxiety disorders: Treatments, models, and circuitry mechanisms
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Neuronal diversity and reciprocal connectivity between the vertebrate hippocampus and septum
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“In addition, it has been suggested that the MS/vDB may also affect affective behaviors ( 10 – 12 ).”
Gruhn, K., Siteneski, A., Camargo, A., Freitas, A. E., Olescowicz, G., Brocardo, P. S., & Rodrigues, A. L. S. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113040 · Cited by 22 · see citing works
Romantic love, pair-bonding, and the dopaminergic reward system.
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“…from romantic love items (“I will love my partner forever.”) and found that activation of the septum-fornix was distinctly related to obsession-related items of the PLS. Lesion studies with rats suggest that it is implicated in anxiety reduction (e.g., Decker et al., 1995; Degroot & Treit, 2004).”
Martin, M. V., Dong, H., Vallera, D., Lee, D., Lu, L., Williams, R. W., Rosen, G. D., Cheverud, J. M., & Csernansky, J. G. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00215.x · Cited by 20 · see citing works
“In rodents, dorsal hippocampus function has been implicated in spatial memory (Pothuizen et al. 2004), while ventral hippocampus function has been implicated in fear and anxiety responses ( Degroot & Treit 2004; Trivedi & Coover 2004).”
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ANI inactivation: Unconditioned anxiolytic effects of anisomycin in the ventral hippocampus
Greenberg, A., Ward-Flanagan, R., Dickson, C. T., & Treit, D. (2014) · Hippocampus · doi:10.1002/hipo.22312 · Cited by 17 · see citing works
“The behavioral effects of ANI infused into the ventral hippocampus were remarkably similar to those using traditional pharmacological inactivators, such as TTX and muscimol (Degroot and Treit, 2004; McEown and Treit, 2010).”
BackgroundMethodInfluentialSelf-citation
- Authors
- Degroot, A., & Treit, D.
- Affiliations
- University of Alberta (CA)
- Corresponding author
- Degroot, Aldemar
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2004-03
- Volume
- 1001
- Issue
- 1-2
- Pages
- 60-71
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2120797053
- Cited by
- 153
- References
- 51
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 1 · 2021: 7 · 2020: 9 · 2019: 2 · 2018: 2 · 2017: 7 · 2016: 5 · 2015: 8 · 2014: 10 · 2013: 9 · 2012: 4
- FWCI
- 4.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- anxiety, septo-hippocampal system, fimbria-fornix, medial septum, dorsal hippocampus, ventral hippocampus, anxiolytic effects, elevated plus maze, functional segregation, amygdala
- MeSH terms
- Analysis of Variance, Anesthetics, Local, Animals, Anxiety, Behavior, Animal, Biotin, Dextrans, Electroshock, Exploratory Behavior, Hippocampus, Male, Reaction Time, Septal Nuclei, Tetrodotoxin, Rats, Sprague-Dawley, Maze Learning, Fornix, Brain, Rats
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