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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

Summary diagram illustrating ascending projections from the dorsolateral PAG to hypothalamic and thalamic targets; these projections influence cortical-hippocampal-amygdalar circuits related to fear learning. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; ECT, ectorhinal area; HF, hippocampal formation; IL, intralaminar nuclei; LA, lateral amygdalar nucleus; LD, laterodorsal thalamic nucleus; PAGdl, periaqueductal gray, dorsolateral part; PERI, perirhinal area; PMd, dorsal premammillary nucleus; RE, nucleus reuniens; RSP, retrosplenial area; SGN, suprageniculate nucleus; SPF, subparafascicular thalamic nucleus; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion. Modified from Kincheski et al. (2012).
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Figure 3: Summary diagram illustrating ascending projections from the dorsolateral PAG to hypothalamic and thalamic targets; these projections influence cortical-hippocampal-amygdalar circuits related to fear learning. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; ECT, ectorhinal area; HF, hippocampal formation; IL, intralaminar nuclei; LA, lateral amygdalar nucleus; LD, laterodorsal thalamic nucleus; PAGdl, periaqueductal gray, dorsolateral part; PERI, perirhinal area; PMd, dorsal premammillary nucleus; RE, nucleus reuniens; RSP, retrosplenial area; SGN, suprageniculate nucleus; SPF, subparafascicular thalamic nucleus; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion. Modified from Kincheski et al. (2012).

Mentions: To understand how the dorsal PAG is able to influence prosencephalic circuits related to fear learning, we revisited the ascending connections of the dorsolateral PAG (Kincheski et al., 2012; Figure 3). The main ascending target of the dorsolateral PAG is the anterior hypothalamic nucleus, which, as described above, is part of the medial hypothalamic predator-responsive circuit. In line with this view, electrical stimulation of the dorsolateral PAG up-regulates Fos expression in the PMd (Vianna et al., 2003), supporting the idea that the PAGdl and the predator-responsive circuit operate in concert. Notably, blockade of PMd beta-adrenergic receptors with atenolol has been shown to impair the acquisition of the olfactory fear learning that is promoted by NMDA stimulation of the dorsal PAG (Kincheski et al., 2012). Thus, the projection from the PAGdl to the medial hypothalamic predator-responsive circuit may serve as an important link by which the prosencephalic sites involved in fear learning can be influenced. In addition, as shown in Figure 3, the PAGdl may potentially influence fear learning through a number of parallel thalamic pathways. The PAGdl provides a substantial projection to the intralaminar nuclei. The intralaminar nuclei, in turn, project to the anterior cingulate area, forming a pathway that is involved in fear learning (Furlong et al., 2010). In addition, the PAGdl also projects to a number of other thalamic sites, including the nucleus reuniens, the lateral dorsal nucleus, the suprageniculate nucleus and the parvicellular subparafascicular nucleus, all of which are known to project to elements of the cortical-hippocampal-amygdalar circuit that is involved in fear conditioning, as described above (Van Groen and Wyss, 1992; Linke et al., 2000; Vertes et al., 2006). An important concept emerges from the present analysis: subcortical regions that process elemental fear to predator threats, such as the PMd and the dorsal PAG, may work as critical nodes that serve to instruct prosencephalic sites to promote fear learning. Accordingly, the processing of primal emotional states related to predatory threats should take place in these subcortical nodes and exert a critical influence on fear learning.


Olfactory instruction for fear: neural system analysis.

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

Summary diagram illustrating ascending projections from the dorsolateral PAG to hypothalamic and thalamic targets; these projections influence cortical-hippocampal-amygdalar circuits related to fear learning. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; ECT, ectorhinal area; HF, hippocampal formation; IL, intralaminar nuclei; LA, lateral amygdalar nucleus; LD, laterodorsal thalamic nucleus; PAGdl, periaqueductal gray, dorsolateral part; PERI, perirhinal area; PMd, dorsal premammillary nucleus; RE, nucleus reuniens; RSP, retrosplenial area; SGN, suprageniculate nucleus; SPF, subparafascicular thalamic nucleus; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion. Modified from Kincheski et al. (2012).
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Figure 3: Summary diagram illustrating ascending projections from the dorsolateral PAG to hypothalamic and thalamic targets; these projections influence cortical-hippocampal-amygdalar circuits related to fear learning. ACA, anterior cingulate area; AHN, anterior hypothalamic nucleus; AMv, anteromedial thalamic nucleus, ventral part; ECT, ectorhinal area; HF, hippocampal formation; IL, intralaminar nuclei; LA, lateral amygdalar nucleus; LD, laterodorsal thalamic nucleus; PAGdl, periaqueductal gray, dorsolateral part; PERI, perirhinal area; PMd, dorsal premammillary nucleus; RE, nucleus reuniens; RSP, retrosplenial area; SGN, suprageniculate nucleus; SPF, subparafascicular thalamic nucleus; VMHdm, ventromedial hypothalamic nucleus, dorsomedial part. See text for discussion. Modified from Kincheski et al. (2012).
Mentions: To understand how the dorsal PAG is able to influence prosencephalic circuits related to fear learning, we revisited the ascending connections of the dorsolateral PAG (Kincheski et al., 2012; Figure 3). The main ascending target of the dorsolateral PAG is the anterior hypothalamic nucleus, which, as described above, is part of the medial hypothalamic predator-responsive circuit. In line with this view, electrical stimulation of the dorsolateral PAG up-regulates Fos expression in the PMd (Vianna et al., 2003), supporting the idea that the PAGdl and the predator-responsive circuit operate in concert. Notably, blockade of PMd beta-adrenergic receptors with atenolol has been shown to impair the acquisition of the olfactory fear learning that is promoted by NMDA stimulation of the dorsal PAG (Kincheski et al., 2012). Thus, the projection from the PAGdl to the medial hypothalamic predator-responsive circuit may serve as an important link by which the prosencephalic sites involved in fear learning can be influenced. In addition, as shown in Figure 3, the PAGdl may potentially influence fear learning through a number of parallel thalamic pathways. The PAGdl provides a substantial projection to the intralaminar nuclei. The intralaminar nuclei, in turn, project to the anterior cingulate area, forming a pathway that is involved in fear learning (Furlong et al., 2010). In addition, the PAGdl also projects to a number of other thalamic sites, including the nucleus reuniens, the lateral dorsal nucleus, the suprageniculate nucleus and the parvicellular subparafascicular nucleus, all of which are known to project to elements of the cortical-hippocampal-amygdalar circuit that is involved in fear conditioning, as described above (Van Groen and Wyss, 1992; Linke et al., 2000; Vertes et al., 2006). An important concept emerges from the present analysis: subcortical regions that process elemental fear to predator threats, such as the PMd and the dorsal PAG, may work as critical nodes that serve to instruct prosencephalic sites to promote fear learning. Accordingly, the processing of primal emotional states related to predatory threats should take place in these subcortical nodes and exert a critical influence on fear learning.

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