Information processing in the vertebrate habenula

Fore, Stephanie; Palumbo, Fabrizio; Pelgrims, Robbrecht; Yaksi, Emre

doi:10.1016/j.semcdb.2017.08.019

Cited by 27 publications

(26 citation statements)

References 169 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The habenula (Hb) plays an important role in operant learning. Mammalian lateral Hb (lHb) receives inputs from various forebrain and midbrain regions and project to the ventral tegmental area (VTA) and raphe nuclei ( Bianco and Wilson, 2009 ; Namboodiri et al., 2016 ; Fore et al., 2018 ; Stamatakis and Stuber, 2012 ; Matsumoto and Hikosaka, 2007 , 2009 ; Lazaridis et al., 2019 ; Trusel et al., 2019 ; Brinschwitz et al., 2010 ; Proulx et al., 2014 ). lHb was shown to encode aversive experiences ( Matsumoto and Hikosaka, 2007 ; Lazaridis et al., 2019 ) and prediction errors ( Trusel et al., 2019 ; Kawai et al., 2015 ).…”

Section: Introductionmentioning

confidence: 99%

“…lHb was shown to encode aversive experiences ( Matsumoto and Hikosaka, 2007 ; Lazaridis et al., 2019 ) and prediction errors ( Trusel et al., 2019 ; Kawai et al., 2015 ). Instead, the medial Hb (mHb) receives inputs from supracommissural septum, VTA, and locus coeruleus and projects to interpeduncular nucleus (IPN) that is connected with the raphe nuclei ( Fore et al., 2018 ; Bianco and Wilson, 2009 ; Namboodiri et al., 2016 ; Hentall and Budhrani, 1990 ; Groenewegen et al., 1986 ). Most studies on mHb focus on its role in depression, anxiety, fear, addiction, and anhedonia ( Yamaguchi et al., 2013 ; Shih et al., 2015 ; Frahm et al., 2011 ).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The Zebrafish Dorsolateral Habenula Is Required for Updating Learned Behaviors

et al. 2020

Self Cite

View full text Add to dashboard Cite

Summary Operant learning requires multiple cognitive processes, such as learning, prediction of potential outcomes, and decision-making. It is less clear how interactions of these processes lead to the behavioral adaptations that allow animals to cope with a changing environment. We show that juvenile zebrafish can perform conditioned place avoidance learning, with improving performance across development. Ablation of the dorsolateral habenula (dlHb), a brain region involved in associative learning and prediction of outcomes, leads to an unexpected improvement in performance and delayed memory extinction. Interestingly, the control animals exhibit rapid adaptation to a changing learning rule, whereas dlHb-ablated animals fail to adapt. Altogether, our results show that the dlHb plays a central role in switching animals’ strategies while integrating new evidence with prior experience.

show abstract

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Zebrafish Dorsolateral Habenula Is Required for Updating Learned Behaviors

et al. 2020

Self Cite

View full text Add to dashboard Cite

show abstract

“…Additionally, habenula neurons constantly fire action potentials, even in the absence of sensory stimulation. This was demonstrated in rats, using electrical recordings of brain slices, and has also been found to be the case in the zebrafish, using two-photon calcium imaging of tethered animals, 19,20 or CaMPARI-based labelling of freely swimming fish. 21 These features -constant activity and the ability to occupy multiple different states -raise the possibility that the habenula may be operating at criticality.…”

Section: Introductionmentioning

confidence: 71%

Percolation in the resting zebrafish habenula

Suryadi

Cheng

Jesuthasan

et al. 2018

Preprint

View full text Add to dashboard Cite

1The habenula is an evolutionarily conserved structure of the vertebrate brain that is essential for behavioural flexibility 2 and mood control. It is spontaneously active and is able to access diverse states when the animal is exposed to sensory 3 stimuli or reward. Here we analyze two-photon calcium imaging time-series of the habenula of larval zebrafish and find 4 that percolation occurs, indicating the presence of long-range spatial correlations within each side of the habenula, with 5 percolation occurring independently in each side. On the other hand, the analysis of neuronal avalanches suggests that the 6 system is subcritical, implying that the flexibility in its dynamics may result from other dynamical processes. 7 130[36]. 131Upon analyzing the pairwise correlation function for the four datasets we observe two distinct behaviors for the power 132 law regime. We saw that the four datasets can be divided into two groups with distinct power law exponents. We note that 133 this may potentially reflect differences in mode of activity of the habenula, or simply be a variation due to the fish itself, 134 which we are unable to determine at this point in time. Nevertheless, the scale invariant behavior of the function suggests 135 long-range spatial correlations among the neurons in the habenula. More importantly, the scale invariant regime extends 136 only up to the scale of any one side of the habenula, which suggests that percolation occurs independently in each side. 137The presence of long-range spatial correlation suggests that the temporal aspect may display critical behavior as well. 138Despite so, our analysis suggests that the habenula are subcritical, i.e. the spatiotemporal neuronal dynamics are less active 139 than the critical state. 140In the absence of criticality, then, how could the habenula achieve its flexibility in terms of accessing different modes 141 of activity? Two possibilities come to mind; the first of which is that the habenula operates not at, but near criticality, as 142 has been suggested in literature [39]. Being near criticality may also explain why we observe the other telltale signs of 143 criticality (including percolation), while failing only the more stringent properties (such as the scaling relation). 144Another possibility lies in our fundamental assumption, which is that only adjacent cells are taken to be connected. 145While it is known that gap junction (which mediates communication among adjacent neurons) are present in habenula 146 7 neurons [40], it could be the case that long-range connections play an important role in the development and transmission 147 of avalanches, i.e. the habenula is actually critical, but we perceive it to be otherwise due to the omission of long-range 148 connections. In such a situation, one large (and long-lasting) avalanche would be perceived as multiple smaller (and 149 potentially shorter) avalanches, causing the probability mass in both distributions to bias towards the left side. Hence, it 150 could explain the sub-power law regim...

show abstract

“…Studies utilizing rodents have indicated that two obvious compartments called medial and lateral HA are distinguishable in HA, and the medial HA contains about 5 subnuclear groups and the lateral HA contains about 10 subnuclear groups (Aizawa et al, 2012;Andres et al, 1999;Klemm, 2004;Sutherland, 1982). This complex composition of HA is a direct reflection of the diverse physiological functions such as feeding, mating, sleep, diet, stress response and aversion or reward processing it involves (Fore et al, 2018;Klemm, 2004;Sandyk, 1991). Comparing to our understanding in the structure, the neurochemical composition and the physiological function of HA, our current knowledge of HA neuronal generation and specification in vertebrate development is relatively limited.…”

Section: Introductionmentioning

confidence: 99%

Three Dimensional Multi-gene Expression Maps Reveal Cell Fate Changes Associated with Laterality Reversal of Zebrafish Habenula

Wang

Pan

Lang

et al. 2020

Preprint

View full text Add to dashboard Cite

ABSTRACTThe conserved bilateral habenular nuclei (HA) in vertebrate diencephalon develop into compartmentalized structures containing neurons derived from different cell lineages. Despite extensive studies demonstrated that zebrafish larval HA display distinct left-right (L-R) asymmetry in gene expression and connectivity, the spatial gene expression domains were mainly obtained from two-dimensional (2D) snapshots of colorimetric RNA in situ hybridization staining which could not properly reflect different HA neuronal lineages constructed in three-dimension (3D). Combing the tyramide-based fluorescent mRNA in situ hybridization, confocal microscopy and customized imaging processing procedures, we have created spatial distribution maps of four genes for 4 day old zebrafish and in sibling fish whose L-R asymmetry was spontaneously reversed. 3D volumetric analyses showed that ratios of cpd2, lov, ron and nrp1a expression in L-R reversed HA were reversed according to the parapineal positions. However, the quantitative changes of gene expression in reversed larval brains do not mirror the gene expression level in the obverse larval brains. There were a total 87.78% increase of lov+nrp1a+ and a total 12.45% decrease of lov+ron+ double-positive neurons when the L-R asymmetry of HA was reversed. Thus, our volumetric analyses of the 3D maps indicate that changes of HA neuronal cell fates are associated with the reversal of HA laterality. These changes likely account for the behavior changes associated with HA laterality alterations.

show abstract

Information processing in the vertebrate habenula

Cited by 27 publications

References 169 publications

The Zebrafish Dorsolateral Habenula Is Required for Updating Learned Behaviors

The Zebrafish Dorsolateral Habenula Is Required for Updating Learned Behaviors

Percolation in the resting zebrafish habenula

Three Dimensional Multi-gene Expression Maps Reveal Cell Fate Changes Associated with Laterality Reversal of Zebrafish Habenula

Contact Info

Product

Resources

About