Tactile mechanisms and afferents underlying the rat pup transport response

Zheyi Ni; Connor Neifert; Arturo Rosete; Abdalla M Albeely; Yu Yang; Marta Pratelli; Michael Brecht; Ann M Clemens

doi:10.1016/j.cub.2024.10.016

Tactile mechanisms and afferents underlying the rat pup transport response

Curr Biol. 2024 Dec 2;34(23):5595-5601.e2. doi: 10.1016/j.cub.2024.10.016. Epub 2024 Nov 4.

Authors

Zheyi Ni¹, Connor Neifert², Arturo Rosete³, Abdalla M Albeely⁴, Yu Yang⁵, Marta Pratelli⁶, Michael Brecht⁷, Ann M Clemens⁸

Affiliations

¹ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Department of Neurobiology, Affiliated Mental Health Center & Hangzhou Seventh People's Hospital and School of Brain Science and Brain Medicine, Zhejiang University School of Medicine, Hangzhou 310058, China.
² Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Department of Bioengineering, University of Texas at Dallas, 800 W Campbell Road, Richardson, TX 75080, USA.
³ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Division of Biological Sciences, University of Missouri, Columbia, MO 65201, USA.
⁴ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Department of Anatomy and Cell Biology, Schulich School of Medicine, Western University, London, ON N6A 5C1, Canada.
⁵ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Department of Mechanical Engineering, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218, USA.
⁶ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Neurobiology Department, School of Biological Sciences and Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, CA 92093-0955, USA; Kavli Institute for Brain and Mind, University of California, San Diego, La Jolla, CA 92093-0955, USA.
⁷ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Philippstr. 13 Haus 6, 10115 Berlin, Germany.
⁸ Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA; University of Edinburgh, Simons Initiative for the Developing Brain, 1 George Square, EH8 9JZ Edinburgh, Scotland, United Kingdom. Electronic address: aclemens@ed.ac.uk.

PMID: 39500320
PMCID: PMC11614678 (available on 2025-12-02)
DOI: 10.1016/j.cub.2024.10.016

Abstract

Juvenile rodents and other altricial mammals react with calming, immobility, and postural modifications to parental pickup, a set of behaviors referred to as the transport response.¹^,²^,³^,⁴^,⁵ Here, we investigate sensory mechanisms underlying the rat transport response. Grasping rat pups in anterior neck positions evokes strong immobility and folding up of feet, whereas more posterior grasping has lesser effects on immobility and foot position. Transport responses are enhanced by slow (1 Hz), and even more so by fast (4 Hz), gentle shaking and translation, features consistent with parental transport. With lateral grasping, the forepaw below the grasping position points downward and the forepaw lateral to the grasping position points upward and medially. Such forepaw adjustments put the pup's center of gravity below the grasping point, optimizing pup transportability. Tactile stimuli on the back, belly, tail, whisker, dorsal forepaws, and dorsal hind-paws do not significantly affect behavior of anterior-neck-held pups. Instead, ground contact, or paw stimulation consistent with ground contact, disrupts transport responses. We identify afferents mediating transport response by examining membrane labeling with FM 1-43⁶ following anterior neck grasping. We observe a dense innervation of the anterior-neck-skin region (∼30 terminals/mm²). We find an age-related decrease of cytochrome oxidase reactivity in the rat somatosensory cortical neck representation, a possible correlate to developmental decrease in pup transport response. We conclude that anterior neck grasping and loss of ground contact trigger calming and postural adjustments for parental transport in rat pups, responses putatively driven from the densely innervated anterior neck skin.

Keywords: calming; immobility; neck afferents; pup retrieval; transport response.

MeSH terms

Animals
Animals, Newborn
Female
Male
Rats
Rats, Long-Evans
Touch* / physiology

Grants and funding

R25 MH059472/MH/NIMH NIH HHS/United States