Multiple behavior-specific cancellation signals contribute to suppressing predictable sensory reafference in a cerebellum-like structure

Movement induces sensory stimulation of an animal's own sensory receptors, termed reafference. With a few exceptions, notably vestibular and proprioception, this reafference is unwanted sensory noise and must be selectively filtered in order to detect relevant external sensory signals. In the cerebellum-like electrosensory nucleus of elasmobranch fish, an adaptive filter preserves novel signals by generating cancellation signals that suppress predictable reafference. A parallel fiber network supplies the principal Purkinje-like neurons (called ascending efferent neurons, AENs) with behavior-associated internal reference signals, including motor corollary discharge and sensory feedback, from which predictive cancellation signals are formed. How distinct behavior-specific cancellation signals interact within AENs when multiple behaviors co-occur and produce complex, changing patterns of reafference is unknown. Here, we show that when multiple streams of internal reference signals are available, cancellation signals form that are specific to parallel fiber inputs temporally correlated with, and therefore predictive of, sensory reafference. A single AEN has the capacity of forming more than one cancellation signal, and AENs form multiple cancellation signals simultaneously and modify them independently during co-occurring behaviors. Cancellation signals update incrementally during continuous behaviors, as well as episodic bouts of behavior that last minutes to hours. Finally, individual AENs, independently of their neighbors, form unique AEN-specific cancellation signals that depend on the particular sensory reafferent input it receives. Together, these results demonstrate the capacity of the adaptive filter to utilize multiple cancellation signals to suppress dynamic patterns of reafference arising from complex co-occurring and intermittently performed behaviors.

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Somatosensory cortical efferent neurons of the awake rabbit: latencies to activation via supra--and subthreshold receptive fields

Journal of Neurophysiology ◽

10.1152/jn.1996.75.4.1753 ◽

1996 ◽

Vol 75 (4) ◽

pp. 1753-1759 ◽

Cited By ~ 16

Author(s):

H. A. Swadlow ◽

T. P. Hicks

Keyword(s):

High Speed ◽

Receptive Fields ◽

Cortical Cell ◽

Sensory Stimulation ◽

Inhibitory Response ◽

Postsynaptic Potentials ◽

Peripheral Stimulation ◽

Efferent Neurons ◽

Excitatory Component ◽

Peripheral Sensory

1. Latencies to peripheral sensory stimulation were examined in four classes of antidromically identified efferent neurons in the primary somatosensory cortex (S1) of awake rabbits. Both suprathreshold responses (action potentials) and subthreshold responses were examined. Subthreshold responses were examined by monitoring the thresholds of efferent neurons to juxtasomal current pulses (JSCPs) delivered through the recording microelectrode (usually 1-3 microA). Through the use of this method, excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) were manifested as decreases and increases in threshold, respectively. Efferent populations examined included callosal (CC) neurons, ipsilateral corticocortical (C-IC) neurons, and descending corticofugal neurons of layer 5 (CF-5) and layer 6 (CF-6). Very brief air puffs (rise and fall times 0.6 ms) were delivered to the receptor periphery via a high-speed solenoid valve. 2. Whereas all CF-5 neurons had demonstrable suprathreshold excitatory and/or inhibitory responses to peripheral stimulation, most CC, C-IC, and CF-6 neurons did not. CC and CF-6 neurons that yielded no suprathreshold response to the stimulus had lower axonal conduction velocities than those that did respond (P < 0.0001 in both cases). However, subthreshold receptive fields could be demonstrated in many of the otherwise unresponsive CC (81%), C-IC (88%), and CF-6 (43%) neurons. The subthreshold responses usually consisted of an initial excitatory component (a decrease in the threshold to the JSCP) and a subsequent long-duration (> 80 ms) inhibitory component. A few neurons (1 CC, 1 C-IC, and 5 CF-6) showed an initial short latency inhibitory response in the absence of any excitatory component. 3. Some CC and C-IC neurons yielded supra- and/or subthreshold responses to peripheral stimulation at latencies of 6.1-7 ms. All such neurons were found at intermediate cortical depths (thought to correspond to deep layer 2-3 through layer 5). It is argued that such latencies are indicative of monosynaptic activation via thalamic afferents. Very superficial CC and C-IC neurons, and all CF-6 neurons responded to latencies of > 7 ms. All CF-5 neurons responded to latencies of > 8 ms, although many were found at the same depth as the deeper CC and C-IC neurons that responded at monosynaptic latencies. These results indicate that cortical cell type as well as laminar position are important factors that determine the sequence of intracortical neuronal activation after peripheral sensory stimulation.

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How Basal Ganglia Outputs Generate Behavior

Advances in Neuroscience ◽

10.1155/2014/768313 ◽

2014 ◽

Vol 2014 ◽

pp. 1-28 ◽

Cited By ~ 14

Author(s):

Henry H. Yin

Keyword(s):

Basal Ganglia ◽

Internal Reference ◽

New Model ◽

Transition Control ◽

Sensorimotor Transformations ◽

Reference Signals ◽

Voluntary Behavior ◽

Functional Hierarchy ◽

Subcortical Nuclei ◽

Output Neurons

The basal ganglia (BG) are a collection of subcortical nuclei critical for voluntary behavior. According to the standard model, the output projections from the BG tonically inhibit downstream motor centers and prevent behavior. A pause in the BG output opens the gate for behavior, allowing the initiation of actions. Hypokinetic neurological symptoms, such as inability to initiate actions in Parkinson’s disease, are explained by excessively high firing rates of the BG output neurons. This model, widely taught in textbooks, is contradicted by recent electrophysiological results, which are reviewed here. In addition, I also introduce a new model, based on the insight that behavior is a product of closed loop negative feedback control using internal reference signals rather than sensorimotor transformations. The nervous system is shown to be a functional hierarchy comprising independent controllers occupying different levels, each level controlling specific variables derived from its perceptual inputs. The BG represent the level of transition control in this hierarchy, sending reference signals specifying the succession of body orientations and configurations. This new model not only explains the major symptoms in movement disorders but also generates a number of testable predictions.

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Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs

Journal of Neurophysiology ◽

10.1152/jn.1994.71.2.437 ◽

1994 ◽

Vol 71 (2) ◽

pp. 437-453 ◽

Cited By ~ 93

Author(s):

H. A. Swadlow

Keyword(s):

Motor Cortex ◽

Receptive Field ◽

Receptive Fields ◽

Sensory Stimulation ◽

Spontaneous Firing ◽

Firing Rates ◽

Axonal Conduction ◽

Conduction Velocities ◽

Efferent Neurons ◽

Stimulation Of

1. Properties of antidromically identified efferent neurons within the cortical representation of the vibrissae, sinus hairs, and philtrum were examined in motor cortex of fully awake adult rabbits. Efferent neurons were tested for both receptive field and axonal properties and included callosal (CC) neurons (n = 31), ipsilateral corticocortical (C-IC) neurons (n = 34) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5) (n = 33) and layer 6 (CF-6) (n = 32) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 37) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrolateral (VL) thalamus and/or S-1 with a burst of three or more spikes at frequencies from 600 to > 900 Hz. All of these neurons also responded synaptically to stimulation of the corpus callosum. The action potentials of these neurons were much shorter in duration (mean = 0.48 ms), than those of efferent neurons (mean = 0.90 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 4.1 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of < 1 spike/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.76 m/s) than either CC (1.47 m/s), C-IC (0.97 m/s), or CF-6 (mean = 1.96 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) followed a single prior impulse in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons. Although all but two CF-5 neurons responded to peripheral sensory stimulation, many CC (35%), C-IC (59%), or CF-6 (66%) neurons did not. CC, CF-5, and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. 4. Sensory receptive fields of neurons in motor cortex were considerably larger than those observed in S-1 but were similar in size to those seen in secondary somatosensory cortex (S-2).(ABSTRACT TRUNCATED AT 400 WORDS)

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Efferent neurons and suspected interneurons in second somatosensory cortex of the awake rabbit: receptive fields and axonal properties

Journal of Neurophysiology ◽

10.1152/jn.1991.66.4.1392 ◽

1991 ◽

Vol 66 (4) ◽

pp. 1392-1409 ◽

Cited By ~ 25

Author(s):

H. A. Swadlow

Keyword(s):

Receptive Field ◽

Corpus Callosum ◽

Somatosensory Cortex ◽

Sensory Stimulation ◽

Spontaneous Firing ◽

Firing Rates ◽

Axonal Conduction ◽

Conduction Velocities ◽

Efferent Neurons ◽

Stimulation Of

1. Receptive-field properties of antidromically identified efferent neurons within the representation of vibrissae and sinus hairs above the mouth were examined in secondary somatosensory cortex (S-2) of fully awake adult rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 88), ipsilateral corticocortical neurons (C-IC neurons, n = 51) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5 neurons, n = 63) and layer 6 (CF-6 neurons, n = 42) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons (21 of 113 tested) project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 62) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-1 and the corpus callosum. The action potentials of these neurons were much shorter (mean, 0.49 ms) than those of efferent neurons (mean, 1.01 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.7 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean, 11.90 m/s) than either CC (mean, 2.63 m/s), C-IC (mean, 0.86 m/s), or CF-6 (mean, 1.73 m/s) neurons. A decrease in antidromic latency (the "supernormal" period), which was dependent on prior impulse activity, was seen in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons of comparable conduction velocity. Although all CF-5 neurons responded to peripheral sensory stimulation, many CC (52%), C-IC (49%), and CF-6 (55%) neurons did not. CC and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. Whereas no CC, C-IC, or CF-6 neuron responded synaptically to callosal stimulation, 43% of CF-5 neurons (and 78% of SINs) did so respond. Similar differences in synaptic responsivity to stimulation of S-1 were seen in these populations.(ABSTRACT TRUNCATED AT 400 WORDS)

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Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties

Journal of Neurophysiology ◽

10.1152/jn.1990.63.6.1477 ◽

1990 ◽

Vol 63 (6) ◽

pp. 1477-1498 ◽

Cited By ~ 39

Author(s):

H. A. Swadlow

Keyword(s):

Receptive Field ◽

Receptive Fields ◽

Sensory Stimulation ◽

Spontaneous Firing ◽

Firing Rates ◽

Axonal Conduction ◽

Receptive Field Properties ◽

Conduction Velocities ◽

Efferent Neurons ◽

Stimulation Of

1. Receptive-field properties of antidromically identified efferent neurons within the cutaneous forelimb representation of primary somatosensory cortex (S-1) were examined in fully awake rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 52), ipsilateral corticocortical neurons (C-IC neurons, n = 48) that project to or beyond the second somatosensory cortical area (S-2), and corticofugal neurons of layer 5 (CF-5 neurons, n = 97) and layer 6 (CF-6 neurons, n = 59) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2 and the corpus callosum. The action potentials of these neurons were much shorter (mean = 0.45 ms) than those of efferent neurons (mean = 0.95 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.5 spikes/s, CC, C-IC, and CF-6 neurons had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.92 m/s) than either CC (mean = 2.15 m/s), C-IC (mean = 1.31 m/s), or CF-6 (mean = 2.53 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) that was dependent on prior impulse activity was seen in the great majority of CC, C-IC, and CF-6 neurons but was either minimal or absent in CF-5 neurons of comparable conduction velocity. A higher proportion of CF-5 neurons (98%) responded to peripheral sensory stimulation than did either CC (75%), C-IC (71%), or CF-6 (51%) neurons. CF-6 and C-IC neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. 4. Cutaneous receptive fields were seen in most neurons that could be driven by peripheral stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

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Physiology of electrosensory lateral line lobe neurons in Gnathonemus petersii

Journal of Experimental Biology ◽

10.1242/jeb.202.10.1301 ◽

1999 ◽

Vol 202 (10) ◽

pp. 1301-1309 ◽

Cited By ~ 1

Author(s):

Y. Sugawara ◽

K. Grant ◽

V. Han ◽

C.C. Bell

Keyword(s):

Lateral Line ◽

Sensory Input ◽

Parallel Fiber ◽

Projection Neurons ◽

Excitatory Postsynaptic Potential ◽

Efferent Neuron ◽

Parallel Fibers ◽

Postsynaptic Potential ◽

Efferent Neurons

In mormyrid electric fish, sensory signals from electroreceptors are relayed to secondary sensory neurons in a cerebellum-like structure known as the electrosensory lateral line lobe (ELL). Efferent neurons and interneurons of the ELL also receive inputs of central origin, including electric organ corollary discharge signals, via parallel fibers and via fibers from the juxtalobar nucleus. To understand the cellular mechanisms of the integration of sensory inputs and central inputs in the ELL, the intracellular activity and ionic properties of the efferent projection neurons and interneurons were examined in an in vitro slice preparation.We focus here on the electrophysiological properties of the efferent neurons of the ELL network, the large fusiform cells and large ganglion cells, and on a class of gamma-aminobutyric acid (GABA)-ergic interneurons known as medium ganglion (MG) cells. In response to current injection through a recording pipette, both types of efferent neuron fire a large narrow spike followed by a large hyperpolarizing afterpotential. The MG cells fire a complex spike which consists of small narrow spikes and a large broad spike. Although the forms of the action potentials in efferent neurons and in MG cells are different, all spikes are mediated by tetrodotoxin (TTX)-sensitive Na+ conductances and spike repolarization is mediated by tetraethylammonium (TEA+)-sensitive K+ conductances. In the presence of TEA+, substitution of Ba2+ for Ca2+ in the bath revealed the presence of a high-voltage-activated Ca2+ conductance.Stimulation of parallel fibers conveying descending input to the ELL molecular layer in vitro evokes an excitatory postsynaptic potential (EPSP), generally followed by an inhibitory postsynaptic potential (IPSP), in the efferent neurons. In MG cells, the same stimulation evokes an EPSP, often followed by a small IPSP. Synaptic transmission at parallel fiber synapses is glutamatergic and is mediated via both N-methyl-d-aspartate (NMDA)- and (AMPA)-type glutamate receptors. The inhibitory component of the parallel fiber response is GABAergic. It is probably mediated via the stellate neurons and the MG cells, which are themselves GABAergic interneurons intrinsic to the ELL network.A hypothetical neural circuit of the intrinsic connections of the ELL, based on the known morphology of projection neurons and medium ganglion interneurons, is presented. This circuit includes an excitatory and an inhibitory submodule. The excitatory submodule is centered on a large fusiform cell and appears to relay the sensory input as a positive ‘ON’ image of an object. The inhibitory submodule is centered on a large ganglion cell and relays a negative ‘OFF’ image to the next higher level. We suggest that MG cells exert an inhibitory bias on efferent neuron types and that the ELL network output is modulated by the dynamically plastic integration of central descending signals with sensory input.

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