Population coding and behavioral choice

Kristan, William B.; Shaw, Brian K.

doi:10.1016/s0959-4388(97)80142-0

Cited by 76 publications

(45 citation statements)

References 38 publications

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“…Addressing this issue will provide insight into the extent to which this system uses convergent activation of the same projection neurons to elicit distinct activity patterns. This would be in contrast to the prevalent hypothesis in other model systems that the generation of distinct but related movements results from the activation of distinct but overlapping sets of projection neurons (Georgopoulos, 1995;Kristan and Shaw, 1997;Lewis and Kristan, 1998;Liu and Fetcho, 1999). …”

Section: Discussioncontrasting

confidence: 74%

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

Blitz

White

Saideman

et al. 2008

Journal of Experimental Biology

144

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SUMMARYNeuronal network flexibility enables animals to respond appropriately to changes in their internal and external states. We are using the isolated crab stomatogastric nervous system to determine how extrinsic inputs contribute to network flexibility. The stomatogastric system includes the well-characterized gastric mill (chewing) and pyloric (filtering of chewed food) motor circuits in the stomatogastric ganglion. Projection neurons with somata in the commissural ganglia (CoGs) regulate these rhythms. Previous work characterized a unique gastric mill rhythm that occurred spontaneously in some preparations, but whose origin remained undetermined. This rhythm includes a distinct protractor phase activity pattern, during which a key gastric mill circuit neuron (LG neuron) and the projection neurons MCN1 and CPN2 fire in a pyloric rhythm-timed activity pattern instead of the tonic firing pattern exhibited by these neurons during previously studied gastric mill rhythms. Here we identify a new extrinsic input, the post-oesophageal commissure (POC) neurons, relatively brief stimulation (30·s) of which triggers a long-lasting (tens of minutes) activation of this novel gastric mill rhythm at least in part via its lasting activation of MCN1 and CPN2. Immunocytochemical and electrophysiological data suggest that the POC neurons excite MCN1 and CPN2 by release of the neuropeptide Cancer borealis tachykinin-related peptide Ia (CabTRP Ia). These data further suggest that the CoG arborization of the POC neurons comprises the previously identified anterior commissural organ (ACO), a CabTRP Ia-containing neurohemal organ. This endocrine organ thus appears to also have paracrine actions, including activation of a novel and lasting gastric mill rhythm.

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Section: Discussioncontrasting

confidence: 74%

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

Blitz

White

Saideman

et al. 2008

Journal of Experimental Biology

144

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“…The fact that both the GPR and VCN neurons activate the gastric mill rhythm via their excitation of MCN1 and CPN2 supports the hypothesis that sensory neurons code for particular behaviors by influencing a subpopulation of the projection neurons that target a particular neuronal circuit (Kristan and Shaw, 1997;Deliagina et al, 2002). The present work also expands our appreciation for the flexibility available to sensory systems that regulate neuronal circuit activity by highlighting that different sensory systems do not require different projection neuron targets to elicit distinct activity patterns from the same neuronal circuit.…”

Section: Discussionmentioning

confidence: 57%

“…Recently, attention has turned to determining how coordinate activation of a population of distinct projection neurons, as can occur via activation of a specific sensory pathway, influences motor circuit output (Combes et al, 1999a,b;Gahtan et al, 2002;. In some motor systems related but distinct sensory cues are thought to elicit different motor outputs as a result of their activation of overlapping but distinct sets of projection neurons (Kristan and Shaw, 1997;Deliagina et al, 2002;Pouget et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Different Sensory Systems Share Projection Neurons But Elicit Distinct Motor Patterns

Blitz

Beenhakker²,

Nusbaum³

2004

J. Neurosci.

122

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Considerable research has focused on issues pertaining to sensorimotor integration, but in most systems precise information remains unavailable regarding the specific pathways by which different sensory systems regulate any single central pattern-generating circuit. We address this issue by determining how two muscle stretch-sensitive neurons, the gastropyloric receptor neurons (GPRs), influence identified projection neurons that regulate the gastric mill circuit in the stomatogastric nervous system of the crab and then comparing these actions with those of the ventral cardiac neuron (VCN) mechanosensory system. Here, we show that the GPR neurons activate the gastric mill rhythm in the stomatogastric ganglion (STG) via their excitation of two identified projection neurons, modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2), in the commissural ganglion. Support for this conclusion comes from the ability of the modulatory proctolin neuron (MPN), a projection neuron that suppresses the gastric mill rhythm via its inhibitory actions on MCN1 and CPN2, to inhibit the GPR-elicited gastric mill rhythm. Selective elimination of MCN1 and CPN2 access to the STG also prevents GPR activation of this rhythm. The VCN neurons also elicit the gastric mill rhythm by coactivating MCN1 and CPN2, but the GPR-elicited gastric mill rhythm is distinct. These distinct rhythms are likely to result partly from different MCN1 activity levels under these two conditions and partly from the presence of additional GPR actions in the STG. These results support the hypothesis that different sensory systems differentially regulate neuronal circuit activity despite their convergent actions on a single subpopulation of projection neurons.

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“…In some systems experimental results indicate that individual sensory inputs diverge to influence many upstream neurons so that the resulting network output results from the pooled activity of a population of these generally not well characterized neurons (Sparks, 1988;Georgopoulos, 1995;Kristan and Shaw, 1997;Lewis, 1999;Pouget et al, 2000;Gold and Shadlen, 2001). This hypothesis, often labeled "population coding," has been suggested to underlie those behaviors that involve a directional response to sensory stimuli (Lewis, 1999), as well as behaviors that are categorically distinct .…”

Section: Introductionmentioning

confidence: 99%

“…With respect to how a sensory signal is transduced into a particular neuronal output, evidence from several systems supports the notion that the "code" is represented by the activity levels and patterns across the population of neurons responsible for eliciting that circuit activity (Berkowitz and Stein, 1994a,b;Laurent, 1996Laurent, , 1997Kristan and Shaw, 1997;Lewis, 1999;Gahtan et al, 2002). This coding scheme has received the most attention in studies involving a directed response (Georgopoulos et al, 1986;Sparks, 1988;Georgopoulos, 1995;Lewis and Kristan, 1998a,b;Lewis, 1999), but it can be extended to include categorically distinct behaviors .…”

mentioning

confidence: 98%

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

Beenhakker¹,

Nusbaum²

2004

J. Neurosci.

102

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Individual neuronal circuits can generate multiple activity patterns because of the influence of different projection neurons. However, in most systems it has been difficult to identify and assess the relative contribution of all upstream neurons responsible for the activation of any single activity pattern by a behaviorally relevant stimulus. To elucidate this issue, we used the stomatogastric nervous system (STNS) of the crab. The STNS includes the gastric mill (chewing) motor circuit in the stomatogastric ganglion (STG) and no more than 20 projection neurons that innervate the STG. We previously identified at least some (four) of the projection neurons that are activated directly by the ventral cardiac neuron (VCN) system, a population of mechanosensory neurons that activates the gastric mill circuit. Here we show that two of these projection neurons, the previously identified modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2), are necessary and likely sufficient for the initiation/maintenance of the VCN-elicited gastric mill rhythm. Selective inactivation of either MCN1 or CPN2 still enabled a VCN-elicited gastric mill rhythm. However, because MCN1 and CPN2 have different actions on gastric mill neurons, these manipulations resulted in rhythms distinct from each other and from that occurring in the intact system. After removal of both MCN1 and CPN2, VCN stimulation failed to activate the gastric mill rhythm. Selective conjoint stimulation of MCN1 and CPN2, approximating their VCN-elicited activity patterns and firing frequencies, elicited a VCN-like gastric mill rhythm. Thus the VCN mechanosensory system elicits the gastric mill rhythm via its activation of a subset of the relevant projection neurons.

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Population coding and behavioral choice

Cited by 76 publications

References 38 publications

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

Different Sensory Systems Share Projection Neurons But Elicit Distinct Motor Patterns

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

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