Cannabinoid mitigation of neuronal morphological change important to development and learning: Insight from a zebra finch model of psychopharmacology

Soderstrom, Ken; Gilbert, Marcoita T.

doi:10.1016/j.lfs.2012.07.031

Cited by 5 publications

(5 citation statements)

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“…This may indicate a more general, CNS-wide role for 2-AG production early in the vocal development period. This possibility is further supported by the general pattern of fiber staining at 25 days that is consistent with endocannabinoid expression within maturing neuronal processes during post-natal development in other species (Soderstrom and Gilbert, 2013). …”

Section: Discussionsupporting

confidence: 58%

Developmental pattern of diacylglycerol lipase-α (DAGLα) immunoreactivity in brain regions important for song learning and control in the zebra finch (Taeniopygia guttata)

Soderstrom

Wilson

2013

Journal of Chemical Neuroanatomy

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Zebra finch song is a learned behavior dependent upon successful progress through a sensitive period of late-postnatal development. This learning is associated with maturation of distinct brain nuclei and the fiber tract interconnections between them. We have previously found remarkably distinct and dense CB1 cannabinoid receptor expression within many of these song control brain regions, implying a normal role for endocannabinoid signaling in vocal learning. Activation of CB1 receptors via daily treatments with exogenous agonist during sensorimotor stages of song learning (but not in adulthood) results in persistent alteration of song patterns. Now we are working to understand physiological changes responsible for this cannabinoid-altered vocal learning. We have found that song-altering developmental treatments are associated with changes in expression of endocannabinoid signaling elements, including CB1 receptors and the principal CNS endogenous agonist, 2-AG. Within CNS, 2-AG is produced largely through activity of the α isoform of the enzyme diacylglycerol lipase (DAGLα). To better appreciate the role of 2-AG production in normal vocal development we have determined the spatial distribution of DAGLα expression within zebra finch CNS during vocal development. Early during vocal development at 25 days, DAGLα staining is typically light and of fibroid processes. Staining peaks late in the sensorimotor stage of song learning at 75 days and is characterized by fiber, neuropil and some staining of both small and large cell somata. Results provide insight to the normal role for endocannabinoid signaling in the maturation of brain regions responsible for song learning and vocal-motor output, and suggest mechanisms by which exogenous cannabinoid exposure alters acquisition of this form of vocal communication.

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Section: Discussionsupporting

confidence: 58%

Developmental pattern of diacylglycerol lipase-α (DAGLα) immunoreactivity in brain regions important for song learning and control in the zebra finch (Taeniopygia guttata)

Soderstrom

Wilson

2013

Journal of Chemical Neuroanatomy

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“…Preliminary results indicate that a similar pattern of Nf-200 expression may occur over normal development, suggesting cannabinoid exposure inhibits normal decreases. Evidence for cannabinoid inhibition of normal CNS developmental processes, and interference with associated morphological change is accumulating for several signaling systems (Soderstrom and Gilbert, 2012). …”

Section: Discussionmentioning

confidence: 99%

“…It has become clear that cannabinoid signaling plays an important modulatory role in establishing neuronal connectivity and morphology both during development and as a function of experience (reviewed by Soderstrom and Gilbert, 2012). This includes regulation of axonal migration (Berghuis et al, 2007) and dendritic structure (Hill et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…This includes regulation of axonal migration (Berghuis et al, 2007) and dendritic structure (Hill et al, 2012). A distinct behavioral sensitivity to cannabinoid exposure during limited periods of peri-adolescent development is also now well-documented (reviewed by Schneider, 2008; Soderstrom and Gilbert, 2012) but physiological mechanisms responsible for these persistent, developmental effects on behavior remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

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Developmental but not adult cannabinoid treatments persistently alter axonal and dendritic morphology within brain regions important for zebra finch vocal learning

Gilbert

Soderstrom

2014

Brain Research

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Prior work shows developmental cannabinoid exposure alters zebra finch vocal development in a manner associated with altered CNS physiology, including changes in patterns of CB1 receptor immunoreactivity, endocannabinoid concentrations and dendritic spine densities. These results raise questions about the selectivity of developmental cannabinoid effects: are they a consequence of a generalized developmental disruption, or are effects produced through more selective and distinct interactions with biochemical pathways that control receptor, endogenous ligand and dendritic spine dynamics? To begin to address this question we have examined effects of developmental cannabinoid exposure on the pattern and density of expression of proteins critical to dendritic (MAP2) and axonal (Nf-200) structure to determine the extent to which dendritic vs. axonal neuronal morphology may be altered. Results demonstrate developmental, but not adult cannabinoid treatments produce generalized changes in expression of both dendritic and axonal cytoskeletal proteins within brain regions and cells known to express CB1 cannabinoid receptors. Results clearly demonstrate that cannabinoid exposure during a period of sensorimotor development, but not adulthood, produce profound effects upon both dendritic and axonal morphology that persist through at least early adulthood. These findings suggest an ability of exogenous cannabinoids to alter general processes responsible for normal brain development. Results also further implicate the importance of endocannabinoid signaling to peri-pubertal periods of adolescence, and underscore potential consequences of cannabinoid abuse during periods of late-postnatal CNS development.

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“…Nevertheless, the tractable nature of zebra finch songs and song control circuits will enable us to understand the detailed neurophysiological mechanisms underlying intrinsic motivation for complex learned motor behaviors. Moreover, endocannabinoids in songbirds are implicated, not only in singing motivation, but also in song development ( Soderstrom and Gilbert, 2013 ; Soderstrom and Johnson, 2003 ), song recognition ( Whitney et al, 2003 ; Hahn et al, 2019 ), and stress responses ( Dickens et al, 2015 ), illustrating the importance of songbirds as a useful model system to study the roles of endocannabinoids in various biological functions.…”

Section: Discussionmentioning

confidence: 99%

Contribution of Endocannabinoids to Intrinsic Motivation for Undirected Singing in Adult Zebra Finches

Kim

Kojima

2022

Front. Physiol.

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Songbirds, such as zebra finches, spontaneously produce many song renditions for vocal practice even in the absence of apparent recipients throughout their lives. Such “undirected singing” is driven by intrinsic motivation, which arises within individuals for internal satisfaction without immediate external rewards. Intrinsic motivation for undirected singing in adult zebra finches was previously demonstrated to be critically regulated by dopamine through D2 receptors. Here, we further investigate the mechanisms of intrinsic motivation for undirected singing by focusing on endocannabinoids, which modulate dopamine signaling and contribute to motivation and reward in mammals. In songbirds, endocannabinoids have been shown to be involved in the production of undirected songs, but whether they are involved in the intrinsic motivation for undirected singing remains unknown. Using latencies of the first song production following temporary singing suppression as a measure of intrinsic motivation for undirected singing, we demonstrate that systemic administration of the direct cannabinoid agonist WIN55212-2 decreases intrinsic motivation for singing and that those effects are largely reversed by the cannabinoid antagonist SR141716A co-administered with WIN55212-2. Administration of SR141716A alone or that of two indirect cannabinoid agonists did not significantly affect intrinsic singing motivation. These results suggest that endocannabinoids are critically involved in regulating intrinsic motivation for undirected singing and provide new insights into the neural mechanisms of intrinsically motivated motor behaviors.

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Cannabinoid mitigation of neuronal morphological change important to development and learning: Insight from a zebra finch model of psychopharmacology

Cited by 5 publications

References 60 publications

Developmental pattern of diacylglycerol lipase-α (DAGLα) immunoreactivity in brain regions important for song learning and control in the zebra finch (Taeniopygia guttata)

Developmental pattern of diacylglycerol lipase-α (DAGLα) immunoreactivity in brain regions important for song learning and control in the zebra finch (Taeniopygia guttata)

Developmental but not adult cannabinoid treatments persistently alter axonal and dendritic morphology within brain regions important for zebra finch vocal learning

Contribution of Endocannabinoids to Intrinsic Motivation for Undirected Singing in Adult Zebra Finches

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