Representation of stimulus speed and direction in vibrissal-sensitive regions of the trigeminal nuclei: A comparison of single unit and population responses

Aniket S. Kaloti, Erik C. Johnson, Chris S. Bresee, Stephanie N. Naufel, Matthew G. Perich, Douglas L Jones, Mitra J.Z. Hartmann

Research output: Contribution to journalArticle

Abstract

The rat vibrissal (whisker) system is one of the oldest and most important models for the study of active tactile sensing and sensorimotor integration. It is well established that primary sensory neurons in the trigeminal ganglion respond to deflections of one and only one whisker, and that these neurons are strongly tuned for both the speed and direction of individual whisker deflections. During active whisking behavior, however, multiple whiskers will be deflected simultaneously. Very little is known about how neurons at central levels of the trigeminal pathway integrate direction and speed information across multiple whiskers. In the present work, we investigated speed and direction coding in the trigeminal brainstem nuclei, the first stage of neural processing that exhibits multi-whisker receptive fields. Specifically, we recorded both single-unit spikes and local field potentials from fifteen sites in spinal trigeminal nucleus interpolaris and oralis while systematically varying the speed and direction of coherent whisker deflections delivered across the whisker array. For 12/15 neurons, spike rate was higher when the whisker array was stimulated from caudal to rostral rather than rostral to caudal. In addition, 10/15 neurons exhibited higher firing rates for slower stimulus speeds. Interestingly, using a simple decoding strategy for the local field potentials and spike trains, classification of speed and direction was higher for field potentials than for single unit spike trains, suggesting that the field potential is a robust reflection of population activity. Taken together, these results point to the idea that population responses in these brainstem regions in the awake animal will be strongest during behaviors that stimulate a population of whiskers with a directionally coherent motion.

Original languageEnglish (US)
Article numbere0158399
JournalPloS one
Volume11
Issue number7
DOIs
StatePublished - Jul 27 2016

Fingerprint

Trigeminal Nuclei
Vibrissae
neurons
Neurons
brain stem
Population
sensory neurons
Brain Stem
taxonomy
Decoding
Direction compound
Spinal Trigeminal Nucleus
Rats
rats
Animals
Trigeminal Ganglion
Touch
Sensory Receptor Cells
animals
Action Potentials

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Representation of stimulus speed and direction in vibrissal-sensitive regions of the trigeminal nuclei : A comparison of single unit and population responses. / Kaloti, Aniket S.; Johnson, Erik C.; Bresee, Chris S.; Naufel, Stephanie N.; Perich, Matthew G.; Jones, Douglas L; Hartmann, Mitra J.Z.

In: PloS one, Vol. 11, No. 7, e0158399, 27.07.2016.

Research output: Contribution to journalArticle

Kaloti, Aniket S. ; Johnson, Erik C. ; Bresee, Chris S. ; Naufel, Stephanie N. ; Perich, Matthew G. ; Jones, Douglas L ; Hartmann, Mitra J.Z. / Representation of stimulus speed and direction in vibrissal-sensitive regions of the trigeminal nuclei : A comparison of single unit and population responses. In: PloS one. 2016 ; Vol. 11, No. 7.
@article{43e03d3b7e9e43bdb8dab19d10c3f41a,
title = "Representation of stimulus speed and direction in vibrissal-sensitive regions of the trigeminal nuclei: A comparison of single unit and population responses",
abstract = "The rat vibrissal (whisker) system is one of the oldest and most important models for the study of active tactile sensing and sensorimotor integration. It is well established that primary sensory neurons in the trigeminal ganglion respond to deflections of one and only one whisker, and that these neurons are strongly tuned for both the speed and direction of individual whisker deflections. During active whisking behavior, however, multiple whiskers will be deflected simultaneously. Very little is known about how neurons at central levels of the trigeminal pathway integrate direction and speed information across multiple whiskers. In the present work, we investigated speed and direction coding in the trigeminal brainstem nuclei, the first stage of neural processing that exhibits multi-whisker receptive fields. Specifically, we recorded both single-unit spikes and local field potentials from fifteen sites in spinal trigeminal nucleus interpolaris and oralis while systematically varying the speed and direction of coherent whisker deflections delivered across the whisker array. For 12/15 neurons, spike rate was higher when the whisker array was stimulated from caudal to rostral rather than rostral to caudal. In addition, 10/15 neurons exhibited higher firing rates for slower stimulus speeds. Interestingly, using a simple decoding strategy for the local field potentials and spike trains, classification of speed and direction was higher for field potentials than for single unit spike trains, suggesting that the field potential is a robust reflection of population activity. Taken together, these results point to the idea that population responses in these brainstem regions in the awake animal will be strongest during behaviors that stimulate a population of whiskers with a directionally coherent motion.",
author = "Kaloti, {Aniket S.} and Johnson, {Erik C.} and Bresee, {Chris S.} and Naufel, {Stephanie N.} and Perich, {Matthew G.} and Jones, {Douglas L} and Hartmann, {Mitra J.Z.}",
year = "2016",
month = "7",
day = "27",
doi = "10.1371/journal.pone.0158399",
language = "English (US)",
volume = "11",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "7",

}

TY - JOUR

T1 - Representation of stimulus speed and direction in vibrissal-sensitive regions of the trigeminal nuclei

T2 - A comparison of single unit and population responses

AU - Kaloti, Aniket S.

AU - Johnson, Erik C.

AU - Bresee, Chris S.

AU - Naufel, Stephanie N.

AU - Perich, Matthew G.

AU - Jones, Douglas L

AU - Hartmann, Mitra J.Z.

PY - 2016/7/27

Y1 - 2016/7/27

N2 - The rat vibrissal (whisker) system is one of the oldest and most important models for the study of active tactile sensing and sensorimotor integration. It is well established that primary sensory neurons in the trigeminal ganglion respond to deflections of one and only one whisker, and that these neurons are strongly tuned for both the speed and direction of individual whisker deflections. During active whisking behavior, however, multiple whiskers will be deflected simultaneously. Very little is known about how neurons at central levels of the trigeminal pathway integrate direction and speed information across multiple whiskers. In the present work, we investigated speed and direction coding in the trigeminal brainstem nuclei, the first stage of neural processing that exhibits multi-whisker receptive fields. Specifically, we recorded both single-unit spikes and local field potentials from fifteen sites in spinal trigeminal nucleus interpolaris and oralis while systematically varying the speed and direction of coherent whisker deflections delivered across the whisker array. For 12/15 neurons, spike rate was higher when the whisker array was stimulated from caudal to rostral rather than rostral to caudal. In addition, 10/15 neurons exhibited higher firing rates for slower stimulus speeds. Interestingly, using a simple decoding strategy for the local field potentials and spike trains, classification of speed and direction was higher for field potentials than for single unit spike trains, suggesting that the field potential is a robust reflection of population activity. Taken together, these results point to the idea that population responses in these brainstem regions in the awake animal will be strongest during behaviors that stimulate a population of whiskers with a directionally coherent motion.

AB - The rat vibrissal (whisker) system is one of the oldest and most important models for the study of active tactile sensing and sensorimotor integration. It is well established that primary sensory neurons in the trigeminal ganglion respond to deflections of one and only one whisker, and that these neurons are strongly tuned for both the speed and direction of individual whisker deflections. During active whisking behavior, however, multiple whiskers will be deflected simultaneously. Very little is known about how neurons at central levels of the trigeminal pathway integrate direction and speed information across multiple whiskers. In the present work, we investigated speed and direction coding in the trigeminal brainstem nuclei, the first stage of neural processing that exhibits multi-whisker receptive fields. Specifically, we recorded both single-unit spikes and local field potentials from fifteen sites in spinal trigeminal nucleus interpolaris and oralis while systematically varying the speed and direction of coherent whisker deflections delivered across the whisker array. For 12/15 neurons, spike rate was higher when the whisker array was stimulated from caudal to rostral rather than rostral to caudal. In addition, 10/15 neurons exhibited higher firing rates for slower stimulus speeds. Interestingly, using a simple decoding strategy for the local field potentials and spike trains, classification of speed and direction was higher for field potentials than for single unit spike trains, suggesting that the field potential is a robust reflection of population activity. Taken together, these results point to the idea that population responses in these brainstem regions in the awake animal will be strongest during behaviors that stimulate a population of whiskers with a directionally coherent motion.

UR - http://www.scopus.com/inward/record.url?scp=85012981918&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85012981918&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0158399

DO - 10.1371/journal.pone.0158399

M3 - Article

C2 - 27463524

AN - SCOPUS:85012981918

VL - 11

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 7

M1 - e0158399

ER -