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Olfactory instruction for fear: neural system analysis.

Canteras NS, Pavesi E, Carobrez AP - Front Neurosci (2015)

Bottom Line: Studies using cat odor have led to detailed mapping of the neural sites involved in innate and contextual fear responses.Here, we reviewed three lines of work examining the dynamics of the neural systems that organize innate and learned fear responses to cat odor.In the first section, we explored the neural systems involved in innate fear responses and in the acquisition and expression of fear conditioning to cat odor, with a particular emphasis on the role of the dorsal premammillary nucleus (PMd) and the dorsolateral periaqueductal gray (PAGdl), which are key sites that influence innate fear and contextual conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo São Paulo, Brazil.

ABSTRACT
Different types of predator odors engage elements of the hypothalamic predator-responsive circuit, which has been largely investigated in studies using cat odor exposure. Studies using cat odor have led to detailed mapping of the neural sites involved in innate and contextual fear responses. Here, we reviewed three lines of work examining the dynamics of the neural systems that organize innate and learned fear responses to cat odor. In the first section, we explored the neural systems involved in innate fear responses and in the acquisition and expression of fear conditioning to cat odor, with a particular emphasis on the role of the dorsal premammillary nucleus (PMd) and the dorsolateral periaqueductal gray (PAGdl), which are key sites that influence innate fear and contextual conditioning. In the second section, we reviewed how chemical stimulation of the PMd and PAGdl may serve as a useful unconditioned stimulus in an olfactory fear conditioning paradigm; these experiments provide an interesting perspective for the understanding of learned fear to predator odor. Finally, in the third section, we explored the fact that neutral odors that acquire an aversive valence in a shock-paired conditioning paradigm may mimic predator odor and mobilize elements of the hypothalamic predator-responsive circuit.

No MeSH data available.


Related in: MedlinePlus

Schematic diagrams showing the putative brain systems that support the encoding (A) and retrieval (B) of learned fear to predator odor. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; BMAp, basomedial amygdalar nucleus, posterior part; ECT, ectorhinal area; HF, hippocampal formation; LA, lateral amygdalar nucleus; LS, lateral septum; MEApv, medial amygdalar nucleus, posteroventral part; PAG, periaqueductal gray; PERI, perirhinal area; PL, prelimbic area; PMd, dorsal premammillary nucleus; RSP, retrosplenial area; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion.
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Figure 2: Schematic diagrams showing the putative brain systems that support the encoding (A) and retrieval (B) of learned fear to predator odor. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; BMAp, basomedial amygdalar nucleus, posterior part; ECT, ectorhinal area; HF, hippocampal formation; LA, lateral amygdalar nucleus; LS, lateral septum; MEApv, medial amygdalar nucleus, posteroventral part; PAG, periaqueductal gray; PERI, perirhinal area; PL, prelimbic area; PMd, dorsal premammillary nucleus; RSP, retrosplenial area; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion.

Mentions: The PMd influences the memory processes that link predatory threats to the associated context. Injection of an NMDA receptor antagonist (2-amino-5-phosphonopentanoic acid) into the PMd during cat odor exposure has been shown to impair conditioned defensive responses to the associated environment (Canteras et al., 2008). Moreover, beta adrenergic blockade in the PMd also reduces contextual fear responses to cat odor (Do Monte et al., 2008). As we shall discuss below, the projection from the PMd to the ventral anteromedial thalamic nucleus (AMv; Canteras and Swanson, 1992; Figure 2A) is a likely pathway to influence mnemonic mechanisms linking predatory threats to their associated context. Recent findings from our group showed that AMv pharmacological inactivation prior to cat exposure did not interfere with innate fear responses but drastically reduced contextual conditioning to the predator-associated environment (De Lima et al., 2013). Thus, the PMd–AMv pathway may be involved in the acquisition of predator-related contextual fear memories. As shown in Figure 2A, the AMv is in a strategic position to convey predator cues to cortico-hippocampal-amygdalar sites involved in the acquisition of contextual fear memories. Previous studies have revealed that the AMv projects to the prelimbic, anterior cingulate, retrosplenial, ectorhinal, and perirhinal cortices as well as to the ventral subiculum and presubiculum (Shibata, 1993; Van Groen et al., 1999). Based on the projection pattern of the AMv, it is clear that this nucleus should exert an important influence on hippocampal processing, either through direct projections to the ventral subiculum and presubiculum or through indirect pathways mediated by the anterior cingulate and retrosplenial areas (Wyss and Van Groen, 1992; Jones and Witter, 2007). The hippocampus is known to be involved in mediating contextual fear memory to predatory threats, and findings from the Blanchard laboratory have shown that ventral hippocampal lesions impair conditioned defensive behaviors associated with either direct exposure to a cat or to its odor (Pentkowski et al., 2006). Moreover, the AMv is also in a position to influence amygdalar sites involved in fear conditioning. As previously noted, the AMv provides moderate input to perirhinal and ectorhinal areas, which are known to provide massive projections to the lateral amygdalar nucleus (Shi and Cassell, 1999). Synapses in the lateral amygdalar nucleus exhibit plasticity that is crucial for fear conditioning (Johansen et al., 2011), and cytotoxic lesions to this region have been shown to block contextual conditioning to predatory threats (Martinez et al., 2011). Taken together, these anatomical findings indicate that the AMv occupies a strategic position to influence both the hippocampus and the lateral amygdalar nucleus, supporting its role in the acquisition of contextual fear memory.


Olfactory instruction for fear: neural system analysis.

Canteras NS, Pavesi E, Carobrez AP - Front Neurosci (2015)

Schematic diagrams showing the putative brain systems that support the encoding (A) and retrieval (B) of learned fear to predator odor. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; BMAp, basomedial amygdalar nucleus, posterior part; ECT, ectorhinal area; HF, hippocampal formation; LA, lateral amygdalar nucleus; LS, lateral septum; MEApv, medial amygdalar nucleus, posteroventral part; PAG, periaqueductal gray; PERI, perirhinal area; PL, prelimbic area; PMd, dorsal premammillary nucleus; RSP, retrosplenial area; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4526802&req=5

Figure 2: Schematic diagrams showing the putative brain systems that support the encoding (A) and retrieval (B) of learned fear to predator odor. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; BMAp, basomedial amygdalar nucleus, posterior part; ECT, ectorhinal area; HF, hippocampal formation; LA, lateral amygdalar nucleus; LS, lateral septum; MEApv, medial amygdalar nucleus, posteroventral part; PAG, periaqueductal gray; PERI, perirhinal area; PL, prelimbic area; PMd, dorsal premammillary nucleus; RSP, retrosplenial area; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion.
Mentions: The PMd influences the memory processes that link predatory threats to the associated context. Injection of an NMDA receptor antagonist (2-amino-5-phosphonopentanoic acid) into the PMd during cat odor exposure has been shown to impair conditioned defensive responses to the associated environment (Canteras et al., 2008). Moreover, beta adrenergic blockade in the PMd also reduces contextual fear responses to cat odor (Do Monte et al., 2008). As we shall discuss below, the projection from the PMd to the ventral anteromedial thalamic nucleus (AMv; Canteras and Swanson, 1992; Figure 2A) is a likely pathway to influence mnemonic mechanisms linking predatory threats to their associated context. Recent findings from our group showed that AMv pharmacological inactivation prior to cat exposure did not interfere with innate fear responses but drastically reduced contextual conditioning to the predator-associated environment (De Lima et al., 2013). Thus, the PMd–AMv pathway may be involved in the acquisition of predator-related contextual fear memories. As shown in Figure 2A, the AMv is in a strategic position to convey predator cues to cortico-hippocampal-amygdalar sites involved in the acquisition of contextual fear memories. Previous studies have revealed that the AMv projects to the prelimbic, anterior cingulate, retrosplenial, ectorhinal, and perirhinal cortices as well as to the ventral subiculum and presubiculum (Shibata, 1993; Van Groen et al., 1999). Based on the projection pattern of the AMv, it is clear that this nucleus should exert an important influence on hippocampal processing, either through direct projections to the ventral subiculum and presubiculum or through indirect pathways mediated by the anterior cingulate and retrosplenial areas (Wyss and Van Groen, 1992; Jones and Witter, 2007). The hippocampus is known to be involved in mediating contextual fear memory to predatory threats, and findings from the Blanchard laboratory have shown that ventral hippocampal lesions impair conditioned defensive behaviors associated with either direct exposure to a cat or to its odor (Pentkowski et al., 2006). Moreover, the AMv is also in a position to influence amygdalar sites involved in fear conditioning. As previously noted, the AMv provides moderate input to perirhinal and ectorhinal areas, which are known to provide massive projections to the lateral amygdalar nucleus (Shi and Cassell, 1999). Synapses in the lateral amygdalar nucleus exhibit plasticity that is crucial for fear conditioning (Johansen et al., 2011), and cytotoxic lesions to this region have been shown to block contextual conditioning to predatory threats (Martinez et al., 2011). Taken together, these anatomical findings indicate that the AMv occupies a strategic position to influence both the hippocampus and the lateral amygdalar nucleus, supporting its role in the acquisition of contextual fear memory.

Bottom Line: Studies using cat odor have led to detailed mapping of the neural sites involved in innate and contextual fear responses.Here, we reviewed three lines of work examining the dynamics of the neural systems that organize innate and learned fear responses to cat odor.In the first section, we explored the neural systems involved in innate fear responses and in the acquisition and expression of fear conditioning to cat odor, with a particular emphasis on the role of the dorsal premammillary nucleus (PMd) and the dorsolateral periaqueductal gray (PAGdl), which are key sites that influence innate fear and contextual conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo São Paulo, Brazil.

ABSTRACT
Different types of predator odors engage elements of the hypothalamic predator-responsive circuit, which has been largely investigated in studies using cat odor exposure. Studies using cat odor have led to detailed mapping of the neural sites involved in innate and contextual fear responses. Here, we reviewed three lines of work examining the dynamics of the neural systems that organize innate and learned fear responses to cat odor. In the first section, we explored the neural systems involved in innate fear responses and in the acquisition and expression of fear conditioning to cat odor, with a particular emphasis on the role of the dorsal premammillary nucleus (PMd) and the dorsolateral periaqueductal gray (PAGdl), which are key sites that influence innate fear and contextual conditioning. In the second section, we reviewed how chemical stimulation of the PMd and PAGdl may serve as a useful unconditioned stimulus in an olfactory fear conditioning paradigm; these experiments provide an interesting perspective for the understanding of learned fear to predator odor. Finally, in the third section, we explored the fact that neutral odors that acquire an aversive valence in a shock-paired conditioning paradigm may mimic predator odor and mobilize elements of the hypothalamic predator-responsive circuit.

No MeSH data available.


Related in: MedlinePlus