Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior

Swanson, Jessica; Ortiz-Guzman, Joshua; Srivastava, Snigdha; Chin, Pey-Shyuan; Dooling, Sean W.; Hanson, Elizabeth; Kochukov, Mikhail Y; Hunt, Patrick J.; Patel, Jay; Pekarek, Brandon; Tong, Qingchun; Arenkiel, Benjamin R.

doi:10.1038/s41598-022-26306-8

Cited by 10 publications

(12 citation statements)

References 75 publications

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“…The behavioral test was conducted in the arena under the same optogenetic stimulation paradigms as in the fMRI experiments to examine the locomotion speed, quiet wakefulness, grooming and object explorations (Figure 5A-C). The VGLUT2-Cre group exhibited a significantly higher locomotion speed (Figure 5D), which was consistent with the wakefulness and avoidance behavior-promoting effect of BF VGLUT2 neurons 3,15,16 . The ChAT-Cre group demonstrated significantly higher novel object explorations (Figure 5E), which is consistent with the involvement of cholinergic systems in attention, learning, and memory 11,12 .…”

Section: Resultssupporting

confidence: 77%

“…The VGLUT2-Cre group exhibited a significantly higher locomotion speed (Fig. 5D), which was consistent with the wakefulness and avoidance behavior-promoting effect of BF VGLUT2 neurons 3,15,16 . The ChAT-Cre group demonstrated significantly higher novel object explorations (Fig.…”

Section: Inhibitory (Pv and Som) Or Excitatory (Vglut2 And Chat) Neur...supporting

confidence: 77%

“…Traditionally, studies of BF have focused on its cholinergic neurons and revealed its involvement in a variety of brain functions, including arousal, attention, memory, learning, motivation and reward both in health and disease [5][6][7][8][9][10][11][12] . However, BF non-cholinergic neurons were also found to contribute to many brain functions 3,[13][14][15][16][17] .…”

Section: Introductionmentioning

confidence: 99%

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Cell-type specific optogenetic fMRI on basal forebrain reveals functional network basis of behavioral preference

Zou

Tong

Peng

et al. 2023

Preprint

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The basal forebrain (BF) is an anatomically and neurochemically complex structure that plays key roles in regulating various brain functions. Although BF is best known for cholinergic neurons that influence functional network dynamics and behaviors, non-cholinergic neurons are the dominant neuronal population in BF, and are found to contribute as well. However, it remains unclear how cholinergic and non-cholinergic BF neurons modulate large-scale functional networks and their relevance in intrinsic and extrinsic behaviors. With our optimized awake mouse optogenetic fMRI approach, we revealed optogenetic stimulations of four BF neuron types evoked distinct cell-type specific whole-brain BOLD activations, which could attribute to BF-originated low dimensional structural networks. Optogenetic activation of inhibitory (PV and SOM) or excitatory (VGLUT2 and ChAT) neurons in BF drove internally or externally oriented behavioral preference, respectively. Furthermore, we uncovered the functional network basis of the above BF-modulated behavioral preference, through a decoding model linking the BF-modulated BOLD activations, low dimensional structural networks, and behavioral preference. To summarize, we decoded a functional network basis of differential behavioral preference with cell-type specific optogenetic fMRI on BF, and provided an avenue for investigating mouse behaviors from a whole-brain view.

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Section: Resultssupporting

confidence: 77%

Section: Inhibitory (Pv and Som) Or Excitatory (Vglut2 And Chat) Neur...supporting

confidence: 77%

Section: Introductionmentioning

confidence: 99%

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Cell-type specific optogenetic fMRI on basal forebrain reveals functional network basis of behavioral preference

Zou

Tong

Peng

et al. 2023

Preprint

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“…Moreover, connections between the BF and basolateral amygdala, lateral habenula (lHb), and lateral hypothalamus may also be involved [31][32][33][34][35].…”

Section: Neuroanatomy Of the Basal Forebrain And Interconnection With...mentioning

confidence: 99%

The Basal Forebrain Serves Social Information Processing

Sobczak,

Bunzeck

2023

Preprint

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Empirical evidence suggests a critical, but little understood, contribution of the cholinergic basal forebrain (BF) to motivational aspects of social cognition. Therefore, we review the current literature on reward and punishment processing in the BF, including social information, in both animals and more recently human imaging studies. This also includes possible interactions with other subcortical structures, especially the ventral striatum and dopaminergic midbrain. Importantly, the BF typically degenerates during healthy and pathological aging, including Parkinson’s disease with dementia, which helps to further understand its role in social information processing. Finally, we suggest a model of cortical and subcortical social information processing (CASSI) bringing together BF contributions in concert with the dopaminergic midbrain and prefrontal cortex to promote social cognition.

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“…Notably, the diagonal band of Broca (DBB) within the basal forebrain is one such node with roles in sensory processing, attention, motivation, and more recently, appetite regulation ( Herman et al, 2016 ; Patel et al, 2019 ). Ablation of cholinergic DBB neurons led to hyperphagia and obesity ( Herman et al, 2016 ), and activation of excitatory DBB neurons downstream of cholinergic neurons led to hypophagia and starvation ( Patel et al, 2019 ; Swanson et al, 2022 ). However, the DBB projects to numerous downstream nodes, and it is unknown which of these may drive the appetite suppression elicited by DBB activation.…”

Section: Introductionmentioning

confidence: 99%

Cholinergic Basal Forebrain Connectivity to the Basolateral Amygdala Modulates Food Intake

Ortiz-Guzman,

Swanson,

Tantry

et al. 2024

eNeuro

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Obesity results from excessive caloric input associated with overeating and presents a major public health challenge. The hypothalamus has received significant attention for its role in governing feeding behavior and body weight homeostasis. However, extra-hypothalamic brain circuits also regulate appetite and consumption by altering sensory perception, motivation, and reward. We recently discovered a population of basal forebrain cholinergic (BFc) neurons that regulate appetite suppression. Through viral tracing methods in the mouse model, we found that BFc neurons densely innervate the basolateral amygdala (BLA), a limbic structure involved in motivated behaviors. Using channelrhodopsin-assisted circuit mapping, we identified cholinergic responses in BLA neurons following BFc circuit manipulations. Furthermore,in vivoacetylcholine sensor and genetically-encoded calcium indicator imaging within the BLA (using GACh3 and GCaMP, respectively) revealed selective response patterns of activity during feeding. Finally, through optogenetic manipulationsin vivo, we found that increased cholinergic signaling from the BFc to the BLA suppresses appetite and food intake. Together, these data support a model in which cholinergic signaling from the BFc to the BLA directly influences appetite and feeding behavior.Significance StatementFeeding behavior has often been associated with homeostatic brain circuits in the hypothalamus. Here we identify a non-homeostatic node of brain circuitry that functions to suppress feeding via cholinergic signaling from the basal forebrain. This circuitry may help explain how mood, motivation, reward, and aversion impacts feeding behavior.

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Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior

Cited by 10 publications

References 75 publications

Cell-type specific optogenetic fMRI on basal forebrain reveals functional network basis of behavioral preference

Cell-type specific optogenetic fMRI on basal forebrain reveals functional network basis of behavioral preference

The Basal Forebrain Serves Social Information Processing

Cholinergic Basal Forebrain Connectivity to the Basolateral Amygdala Modulates Food Intake

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