Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation.
Although peripheral deafferentation studies have demonstrated a critical role for trigeminal afference in modulating the orosensorimotor control of eating and drinking, the central trigeminal pathways mediating that control, as well as the timescale of control, remain to be elucidated. In rodents, t...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0258837 |
| _version_ | 1817980805021958144 |
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| author | Admir Resulaj Jeannette Wu Mitra J Z Hartmann Paul Feinstein H Phillip Zeigler |
| author_facet | Admir Resulaj Jeannette Wu Mitra J Z Hartmann Paul Feinstein H Phillip Zeigler |
| author_sort | Admir Resulaj |
| collection | DOAJ |
| description | Although peripheral deafferentation studies have demonstrated a critical role for trigeminal afference in modulating the orosensorimotor control of eating and drinking, the central trigeminal pathways mediating that control, as well as the timescale of control, remain to be elucidated. In rodents, three ascending somatosensory pathways process and relay orofacial mechanosensory input: the lemniscal, paralemniscal, and extralemniscal. Two of these pathways (the lemniscal and extralemniscal) exhibit highly structured topographic representations of the orofacial sensory surface, as exemplified by the one-to-one somatotopic mapping between vibrissae on the animals' face and barrelettes in brainstem, barreloids in thalamus, and barrels in cortex. Here we use the Prrxl1 knockout mouse model (also known as the DRG11 knockout) to investigate ingestive behavior deficits that may be associated with disruption of the lemniscal pathway. The Prrxl1 deletion disrupts somatotopic patterning and axonal projections throughout the lemniscal pathway but spares patterning in the extralemniscal nucleus. Our data reveal an imprecise and inefficient ingestive phenotype. Drinking behavior exhibits deficits on the timescales of milliseconds to seconds. Eating behavior shows deficits over an even broader range of timescales. An analysis of food acquisition and consummatory rate showed deficits on the timescale of seconds, and analysis of body weight suggested deficits on the scale of long term appetitive control. We suggest that ordered assembly of trigeminal sensory information along the lemniscal pathway is critical for the rapid and precise modulation of motor circuits driving eating and drinking action sequences. |
| first_indexed | 2024-04-13T22:57:50Z |
| format | Article |
| id | doaj.art-a7a5480b55d047a99ebbd3638c564f31 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-04-13T22:57:50Z |
| publishDate | 2022-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-a7a5480b55d047a99ebbd3638c564f312022-12-22T02:25:57ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01174e025883710.1371/journal.pone.0258837Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation.Admir ResulajJeannette WuMitra J Z HartmannPaul FeinsteinH Phillip ZeiglerAlthough peripheral deafferentation studies have demonstrated a critical role for trigeminal afference in modulating the orosensorimotor control of eating and drinking, the central trigeminal pathways mediating that control, as well as the timescale of control, remain to be elucidated. In rodents, three ascending somatosensory pathways process and relay orofacial mechanosensory input: the lemniscal, paralemniscal, and extralemniscal. Two of these pathways (the lemniscal and extralemniscal) exhibit highly structured topographic representations of the orofacial sensory surface, as exemplified by the one-to-one somatotopic mapping between vibrissae on the animals' face and barrelettes in brainstem, barreloids in thalamus, and barrels in cortex. Here we use the Prrxl1 knockout mouse model (also known as the DRG11 knockout) to investigate ingestive behavior deficits that may be associated with disruption of the lemniscal pathway. The Prrxl1 deletion disrupts somatotopic patterning and axonal projections throughout the lemniscal pathway but spares patterning in the extralemniscal nucleus. Our data reveal an imprecise and inefficient ingestive phenotype. Drinking behavior exhibits deficits on the timescales of milliseconds to seconds. Eating behavior shows deficits over an even broader range of timescales. An analysis of food acquisition and consummatory rate showed deficits on the timescale of seconds, and analysis of body weight suggested deficits on the scale of long term appetitive control. We suggest that ordered assembly of trigeminal sensory information along the lemniscal pathway is critical for the rapid and precise modulation of motor circuits driving eating and drinking action sequences.https://doi.org/10.1371/journal.pone.0258837 |
| spellingShingle | Admir Resulaj Jeannette Wu Mitra J Z Hartmann Paul Feinstein H Phillip Zeigler Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. PLoS ONE |
| title | Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. |
| title_full | Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. |
| title_fullStr | Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. |
| title_full_unstemmed | Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. |
| title_short | Impaired trigeminal control of ingestive behavior in the Prrxl1-/- mouse is associated with a lemniscal-biased orosensory deafferentation. |
| title_sort | impaired trigeminal control of ingestive behavior in the prrxl1 mouse is associated with a lemniscal biased orosensory deafferentation |
| url | https://doi.org/10.1371/journal.pone.0258837 |
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