Rat cerebellar cortex in vitro responds specifically to moving stimuli
Abstract
In spite of the detailed anatomical knowledge available, the functional significance of the cerebellar wiring diagram is still obscure. Since there are no variations in the anatomy throughout the whole cortical plane, it is plausible to assume that the basic operation is the same in all parts of the cerebellum. The 'wiring' suggests that local activity must depend on the spatio-temporal organization of the inputs. Neocortical input reaches the cerebellar cortex from nearly all cortical areas via mossy fibers terminating on the granular cells. We simulated such an input to the granular layer in acute slices of rat cerebellar cortex using an array of 11 stimulating electrodes. By successively switching the stimulus current from one electrode to the next, a 'moving' input to the granular layer is simulated. Our experiments show that the cerebellar cortex is specifically activated by 'moving' stimuli applied to the granular layer. The activation is a function of 'movement' direction and velocity. Thus, it enables the cerebellar cortex to act as a movement detector. Such behavior has previously been postulated on anatomical grounds [Braitenberg, J. Theoret. Neurobiol., 2 (1983) 237-241; Braitenberg, In Glickstein et al. (Eds.), Cerebellum and Neuronal Plasticity, Plenum, 1987, pp. 193-207].
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The specific arrangement of parallel fibers and Purkinje cells in cerebellar cortex forms a network that detects precisely timed sequences of input activity and generates precisely timed output activity.
“The specific arrangement of parallel fibers and Purkinje cells in the cerebellar cortex forms a network that specifically detects precisely timed sequences of input activity and generates precisely timed output activity in response [223–225].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [223]
Cites
Synaptic‐ and agonist‐induced excitatory currents of Purkinje cells in rat cerebellar slices.
Llano, I., Marty, A., Armstrong, C. M., & Konnerth, A. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018465 · Cited by 482 · see citing works
Bower, J. M., & Woolston, D. C. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.3.745 · Cited by 360 · see citing works
Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum
Eccles, J. C., Llin�s, R., & Sasaki, K. S. (1966) · Experimental Brain Research · doi:10.1007/bf00235207 · Cited by 302 · see citing works
Crépel, F., Dhanjal, S. S., & Sears, T. A. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014304 · Cited by 213 · see citing works
Cerebellum and Neuronal Plasticity
Glickstein, M., Yeo, C. H., & Stein, J. F. (1987) · Springer eBooks · doi:10.1007/978-1-4613-0965-9 · Cited by 127 · see citing works
Llinas, R. H. (1982) · Experimental brain research. Supplementum · doi:10.1007/978-3-642-68560-6_10 · Cited by 108 · see citing works
Morphological and electrophysiological characteristics of rat cerebellar slices maintained in vitro.
Crépel, F., Dhanjal, S. S., & Garthwaite, J. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013777 · Cited by 65 · see citing works
Braitenberg, V. (1983) · MPG.PuRe (Max Planck Society) · Cited by 46 · see citing works
The Cerebellum And The Physics Of Movement: Some Speculations
Braitenberg, V. (1987) · Springer eBooks · doi:10.1007/978-1-4613-0965-9_13 · Cited by 45 · see citing works
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Consensus Paper: Pathological Role of the Cerebellum in Autism
Fatemi, S. H., Aldinger, K. A., Ashwood, P., Bauman, M. L., Blaha, C. D., Blatt, G. J., Chauhan, A., Chauhan, V., Dager, S. R., Dickson, P. E., et al. (2012) · The Cerebellum · doi:10.1007/s12311-012-0355-9 · Cited by 723 · see citing works
Self-citationThe detection and generation of sequences as a key to cerebellar function: Experiments and theory
Braitenberg, V., Heck, D., & Sultan, F. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x9700143x · Cited by 298 · see citing works
Self-citationThach, W. T. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081504 · Cited by 274 · see citing works
On climbing fiber signals and their consequence(s)
Simpson, J. I., WYLIE, D. R. W., & Zeeuw, C. I. D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081486 · Cited by 247 · see citing works
Use of voltage-sensitive dyes and optical recordings in the central nervous system
Ebner, T. J., & Chen, G. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)00010-s · Cited by 210 · see citing works
Frey, U., Egert, U., Heer, F., Hafizovic, S., & Hierlemann, A. R. (2008) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2008.11.028 · Cited by 202 · see citing works
“Acute slice preparations Parasagittal cerebellar slices (0.3 mm thick) were prepared rom Long-Evans rats at postnatal days 16–18 as described preiously (Heck, 1993).”
MethodInfluentialNaber, P. A., & Witter, M. P. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980413)393:3 · Cited by 219 · see citing works
On-beam synchrony in the cerebellum as the mechanism for the timing and coordination of movement
Heck, D. H., Thach, W. T., & Keating, J. G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609966104 · Cited by 133 · see citing works
Self-citationTwo-dimensional monitoring of spiking networks in acute brain slices
Egert, U., Heck, D. H., & Aertsen, A. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0932-5 · Cited by 122 · see citing works
Self-citationHeck, D. (1995) · Naturwissenschaften · doi:10.1007/bf01143198 · Cited by 69 · see citing works
Self-citationCerebellar Coordination of Neuronal Communication in Cerebral Cortex
McAfee, S. S., Liu, Y., Sillitoe, R. V., & Heck, D. H. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.781527 · Cited by 60 · see citing works
“…network can indeed transform sequential input arriving at the GC layer into synchronous volleys of parallel fiber spikes and elicit sequence specific Purkinje cell responses was shown in a series of in vitro experiments by one of us (Heck, 1993, 1995, 1999; see also Braitenberg et al., 1997).”
BackgroundSelf-citationEyeblink conditioning, motor control, and the analysis of limbic-cerebellar interactions
Weiss, C., & Disterhoft, J. F. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081929 · Cited by 52 · see citing works
Sultan, F. R. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01593.x · Cited by 49 · see citing works
“All of this mediolateral spread of activity would then result in a total of 70-mm mediolateral smearing in the parallel ®bre input, which would correspond to about 233 ms of smearing in the temporal domain (assuming a parallel ®bre conduction velocity of about 0.3 mm/ms, Heck, 1993).”
MethodInfluentialHanson, C. L., Chen, G., & Ebner, T. J. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00470-4 · Cited by 49 · see citing works
Schutter, E. D. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.504 · Cited by 41 · see citing works
Cerebellar structure and function: Making sense of parallel fibers
Heck, D. H., & Sultan, F. R. (2002) · Human Movement Science · doi:10.1016/s0167-9457(02)00123-9 · Cited by 38 · see citing works
“The only excitatory fibers within the cerebellar cortex are the thin, unmyelinated and slowly conducting (0.5 m/s) parallel fibers (Eccles et al., 1967; Heck, 1993), which run in parallel (hence their name) in a latero-lateral direction.”
BackgroundInfluentialSelf-citationSchmahmann, J. D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081851 · Cited by 36 · see citing works
Sensory prediction as a role for the cerebellum
Miall, R. C., Malkmus, M., & Robertson, E. M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081796 · Cited by 29 · see citing works
Sultan, F. R. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00984-2 · Cited by 27 · see citing works
Sultan, F. R., & Heck, D. H. (2003) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2004.01.016 · Cited by 24 · see citing works
Self-citationCerebellar theory out of control
Paulin, M. G. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081838 · Cited by 24 · see citing works
Thach, W. T. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00082017 · Cited by 24 · see citing works
Exploring the significance of morphological diversity for cerebellar granule cell excitability
Houston, C. M., Diamanti, E. M., Diamantaki, M., Kutsarova, E., Cook, A. A., Sultan, F. R., & Brickley, S. G. (2017) · Scientific Reports · doi:10.1038/srep46147 · Cited by 23 · see citing works
The common inverse-dynamics motor-command coordinates for complex and simple spikes
Kawato, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081760 · Cited by 22 · see citing works
Sequence Detectors as a Basis of Grammar in the Brain
Friedemann Pulvermüller, A. (2003) · Theory in Biosciences · doi:10.1007/s12064-003-0039-6 · Cited by 20 · see citing works
Heck, D. H. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)00161-9 · Cited by 18 · see citing works
Self-citationBraitenberg, V. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb07565.x · Cited by 16 · see citing works
More on climbing fiber signals and their consequence(s)
Simpson, J. I., WYLIE, D. R. W., & Zeeuw, C. I. D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081991 · Cited by 13 · see citing works
Computational significance of the cellular mechanisms for synaptic plasticity in Purkinje cells
Houk, J. C., & Alford, S. T. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081735 · Cited by 11 · see citing works
Motor learning and synaptic plasticity in the cerebellum
Thompson, R. F. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081887 · Cited by 9 · see citing works
From Cortical Maps to the Control of Muscles
Morasso, P., & Sanguineti, V. (1997) · Advances in psychology · doi:10.1016/s0166-4115(97)80018-0 · Cited by 9 · see citing works
Perhaps it's time to completely rethink cerebellar function
Bower, J. M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081553 · Cited by 9 · see citing works
Heck, D. H. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00138-x · Cited by 9 · see citing works
“Furthermore, the presented results add to and confirm earlier reports of the cerebellum responding specifically to ‘moving’ input [9,11], a mechanism that might play an important role in motor control [4].”
BackgroundResultSelf-citationFlament, D., & Ebner, T. J. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081620 · Cited by 8 · see citing works
Heck, D. H., Sultan, F. R., & Braitenberg, V. (2001) · Neurocomputing · doi:10.1016/s0925-2312(01)00421-0 · Cited by 7 · see citing works
Self-citationFeldman, A. G., & Levin, M. F. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081607 · Cited by 6 · see citing works
Control of Functional Connectivity in Cerebral Cortex by Basal Ganglia Mediated SynchronizationPreprint
Pouzzner, D. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1708.00779 · Cited by 6 · see citing works
“Heck D, Sultan F (2002). Cerebellar structure and function:”
BackgroundTwo separate pathways for cerebellar LTD: NO-dependent and NO-independent
Hartell, N. A. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081681 · Cited by 4 · see citing works
What has to be learned in motor learning?
Harold Bekkering, A., Heck, D. H., & Sultan, F. R. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0008153x · Cited by 4 · see citing works
Self-citationSchutter, E. D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081577 · Cited by 4 · see citing works
Limitations of PET and lesion studies in defining the role of the human cerebellum in motor learning
Timmann, D., & Diener, H. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081899 · Cited by 4 · see citing works
What behavioral benefit does stiffness control have? An elaboration of Smith's proposal
van Galen, G. P., Hendriks, A. W. C. J., & DeJong, W. P. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081917 · Cited by 4 · see citing works
Effect of Ecological Pressures on Brains: Examples from Avian Neuroethology and General Meanings
Wagner, H., & Luksch, H. (1998) · Zeitschrift für Naturforschung C · doi:10.1515/znc-1998-7-810 · Cited by 4 · see citing works
Spanning the levels in cerebellar function
Arbib, M. A. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081516 · Cited by 3 · see citing works
Long-term changes of synaptic transmission: A topic of long-term interest
Calabresi, P., Pisani, A., & Bernardi, G. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081565 · Cited by 3 · see citing works
Cerebellar rhythms: Exploring another metaphor
Roberts, P. D., McCollum, G., & Holly, J. E. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0008184x · Cited by 3 · see citing works
Houk, J. C., & Barto, A. G. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0008198x · Cited by 3 · see citing works
Similarities and contrasts between cerebellar LTD and hippocampal LTP
Baudry, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081528 · Cited by 3 · see citing works
Positive cerebellar feedback loops
Hesslow, G. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0008170x · Cited by 3 · see citing works
From cerebellar texture to movement optimization
Sultan, F. R. (2014) · Biological Cybernetics · doi:10.1007/s00422-014-0618-2 · Cited by 2 · see citing works
The Functional Significance of Cerebellar Anatomy
Heck, D. H. (1996) · Springer eBooks · doi:10.1007/978-1-4615-5899-6_24 · Cited by 2 · see citing works
“All experiments mentioned here were done in acute slices prepared from rat or guinea pig cerebellar cortices (Heck, 1993b; Heck, 1993a; Heck & Braitenberg, 1993; Heck, 1995a; Heck, 1995c).”
BackgroundMethodSelf-citationTiming implications of metabotropic mechanisms for cerebellar learning
Fiala, J. C., & Bullock, D. H. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081619 · Cited by 2 · see citing works
Cerebellum does more than recalibration of movements after perturbations
Gielen, C. C. A. M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081632 · Cited by 2 · see citing works
Is stiffness a byproduct or a target?
Gomi, H. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081656 · Cited by 2 · see citing works
No more news from the cerebellum
Vincent, S. R. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081978 · Cited by 2 · see citing works
The role of the cerebellum in motor learning is limited
Hallett, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0008167x · Cited by 2 · see citing works
Cerebellar arm ataxia: Theories still have a lot to explain
Hore, J. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081723 · Cited by 2 · see citing works
How and what does the cerebellum learn?
Gilbert, P. F. C. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081644 · Cited by 2 · see citing works
Saccades and the adjustable pattern generator
Dean, P. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081589 · Cited by 2 · see citing works
Kano, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081966 · Cited by 2 · see citing works
Mori-Okamoto, J., & Okamoto, K. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081802 · Cited by 1 · see citing works
Subcellular-resolution recording of electrical activity using a CMOS-microelectroode system
Frey, U., Egert, U., Heer, F., Hafizovic, S., & Hierlemann, A. R. (2009) · International Conference on Solid-State Sensors, Actuators and Microsystems · doi:10.1109/sensor.2009.5285753 · Cited by 1 · see citing works
“3 mm thick) were prepared from Long-Evans rats at postnatal days 16–18 as described previously [10].”
MethodThe notions of joint stiffness and synaptic plasticity in motor memory
Latash, L. P., & Latash, M. L. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081784 · Cited by 1 · see citing works
Anatomical structure alone cannot predict function
Jaeger, D., & Schutter, E. D. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x97311431 · Cited by 1 · see citing works
How to link the specificity of cerebellar anatomy to motor learning?
Sultan, F. R., Heck, D. H., & Harold Bekkering, A. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081863 · Cited by 1 · see citing works
Self-citationWe know a lot about the cerebellum, but do we know what motor learning is?
Swinnen, S. P., Walter, C. B., & Dounskaia, N. V. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081875 · Cited by 1 · see citing works
A cerebellar long-term depression update
Linden, D. J. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081942 · Cited by 1 · see citing works
Cellular mechanisms of long-term depression: From consensus to open questions
Crépel, F. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081954 · Cited by 1 · see citing works
Nitric oxide is involved in cerebellar long-term depression
Okada, D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081814 · Cited by 1 · see citing works
Resilient cerebellar theory complies with stiff opposition
Smith, A. M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00082005 · Cited by 1 · see citing works
Which cerebellar cells contribute to extracellular cGMP?
Kiedrowski, L. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081772 · Cited by 1 · see citing works
New players for cerebellar long-term depression
Kano, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081759 · Cited by 1 · see citing works
Constructing a theory of cerebellar function in limb movement control is premature
Jaeger, D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081747 · Cited by 1 · see citing works
O’Mara, S. M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081826 · Cited by 1 · see citing works
Molecules involved in cerebellar long-term depression (LTD) and mutant mice defective in it
Hirano, T. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081711 · Cited by 1 · see citing works
How can the cerebellum match “error signal” and “error correction”?
Dufossé, M. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081590 · Cited by 1 · see citing works
Hepp, K. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081693 · Cited by 1 · see citing works
Sensorimotor learning in structures “upstream” from the cerebellum
van Donkelaar, P. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081905 · Cited by 1 · see citing works
Plasticity of cerebro-cerebellar interactions in patients with cerebellar dysfunction
Wessel, K. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081930 · Cited by 1 · see citing works
LUTION RECORDING OF ELECTRICAL A CMOS-MICROELECTRODE SYSTEM
Frey, U., Eg, U., de Heer, F. J., Hafizovic, S., & Hierlemann, A. R. (2009)
What can and what cannot be adjusted in the movement patterns of cerebellar patients?
Haggard, P. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081668
Bindman, L. J. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081541
- Authors
- Heck, D.
- Affiliations
- Max Planck Institute for Biological Cybernetics (DE)
- Corresponding author
- Heck, Detlef
- ORCID
- Heck, Detlef
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 1993-07
- Volume
- 157
- Issue
- 1
- Pages
- 95-98
- ISSN
- 0304-3940 (ISSN-L)
- OpenAlex
- W2029166980
- Cited by
- 82
- References
- 9
- Citations by year
- 2022: 1 · 2017: 2 · 2014: 1 · 2012: 1
- FWCI
- 11.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- cerebellar cortex, granular layer, moving stimuli, motion detection, mossy fibers, granular cells, movement direction, movement speed, in vitro slice preparation
- MeSH terms
- Animals, Cerebellar Cortex, Electric Stimulation, Electrophysiology, Evoked Potentials, Nerve Fibers, Quinoxalines, Tetrodotoxin, Rats, Sprague-Dawley, 6-Cyano-7-nitroquinoxaline-2,3-dione, Rats, In Vitro Techniques
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