Degradation of head direction cell activity during inverted locomotion.
Head direction (HD) cells in the rat limbic system carry information about the direction the head is pointing in the horizontal plane. Most previous studies of HD functioning have used animals locomoting in an upright position or ascending/descending a vertical wall. In the present study, we recorded HD cell activity from the anterodorsal thalamic nucleus while the animal was locomoting in an upside-down orientation. Rats performed a shuttle-box task requiring them to climb a vertical wall and locomote across the ceiling of the apparatus while inverted to reach an adjoining wall before ascending into the reward compartment. The apparatus was oriented toward the preferred direction of the recorded cell, or the 180 degrees opposite direction. When the animal was traversing the vertical walls of the apparatus, the HD cells remained directionally tuned as if the walls were an extension of the floor. When the animal was locomoting inverted on the ceiling, however, cells showed a dramatic change in activity. Nearly one-half (47%) of the recorded cells exhibited no directional specificity during inverted locomotion, despite showing robust directional tuning on the walls before and after inversion. The remaining cells showed significantly degraded measures of directional tuning and random shifts of the preferred direction relative to the floor condition while the animal was inverted. It has previously been suggested that the HD system uses head angular velocity signals from the vestibular system to maintain a consistent representation of allocentric direction. These findings suggest that being in an inverted position causes a distortion of the vestibular signal controlling the HD system.
Calton
Jeffrey L
JL
Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire 03755, USA.
Taube
Jeffrey S
JS
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D020643:Anterior Thalamic Nuclei / Q000166:cytology; D001522:Behavior, Animal; D005260:Female; D019416:Head Movements / Q000502:physiology*; D008124:Locomotion / Q000502:physiology*; D009043:Motor Activity / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009949:Orientation; D051381:Rats; D020318:Rats, Long-Evans
Am J Otol. 1999 Nov;20(6):735-40
10565717
J Neurophysiol. 2000 Jan;83(1):393-405
10634882
J Neurophysiol. 2000 Jun;83(6):3402-10
10848558
Exp Brain Res. 2000 Jun;132(4):434-44
10912824
Trends Neurosci. 2001 May;24(5):289-94
11311382
Behav Neurosci. 2001 Apr;115(2):285-304
11345955
Behav Neurosci. 2001 Jun;115(3):571-88
11439447
J Neurosci. 2001 Aug 1;21(15):5740-51
11466446
Adv Neural Inf Process Syst. 1995;7:173-80
11539168
Hippocampus. 2002;12(3):291-303
12099481
J Physiol. 1960 Sep;153:350-7
13782901
Cereb Cortex. 2003 Nov;13(11):1162-72
14576208
J Neurophysiol. 2004 Nov;92(5):2887-997
15212426
Behav Cogn Neurosci Rev. 2002 Dec;1(4):297-317
17712986
J Neurosci. 1990 Feb;10(2):436-47
2303852
Exp Brain Res. 1978 Apr 14;31(4):573-90
658182
Physiol Behav. 1984 Jan;32(1):115-8
6718521
J Neurosci. 1995 Jan;15(1 Pt 1):70-86
7823153
J Neurophysiol. 1994 Mar;71(3):1222-49
8201414
J Neurophysiol. 1993 Jun;69(6):2039-55
8350132
J Neurophysiol. 1995 Nov;74(5):1953-71
8592189
J Neurosci. 1996 Mar 15;16(6):2112-26
8604055
Hippocampus. 1996;6(6):720-34
9034858
J Neurosci. 1997 Jun 1;17(11):4349-58
9151751