Cellular and Behavioral Properties of Learning in Leech and Other Annelids

Crisp, Kevin M.; Burrell, Brian D.

doi:10.1002/9780470455203.ch8

Cited by 9 publications

(8 citation statements)

References 129 publications

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“…(The results of clustering were not consistent among local bending trials. This may stem from a nature of this reflex behavior: there are variability of responsiveness of population of neurons involving pressure sensation, which can reflect plasticity of the reflex circuit (Crisp and Burrell, 2009).) In agreement with earlier reports (Kleindienst et al, 2011), the strongest correspondence between spatial clusters and activity patterns was observed when synaptic clusters were defined by a maximum distance between nearest neighbors (d NN ) of up to 10 μm.…”

Section: Discussionsupporting

confidence: 89%

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Ashaber

Tomina

Kassraian-Fard

et al. 2020

Preprint

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In most animal phyla, nerve cells form highly specific connections with each other 1,2 . The resulting intricate networks determine what activity patterns a nervous system can sustain, and hence what behaviors an animal can exhibit 3,4 . Accordingly, understanding the relationship between connectivity and activity is a major goal of neuroscience. However, despite major recent advances 5,6 , no current technology can comprehensively record activity in large nervous systems such as the human or even the mouse brain, nor can connectivity be reconstructed at synaptic level in such systems 7 . Doing both at once in the same specimen remains a distant goal.However, smaller nervous systems offer exciting opportunities today, and here we report for the first time obtaining joint functional and anatomical data from a major functional unit of the nervous system of the medicinal leech, by combining voltage-sensitive dye (VSD) 8 imaging with serial blockface electron microscopy (SBEM) 9 . We simultaneously recorded from the majority of the neurons in a segmental ganglion during several motor behaviors with a VSD sufficiently sensitive to record subthreshold neuronal activity 10,11 . We then anatomically imaged the entire ganglion with SBEM 12 . As a proof of concept, we have manually traced a critical motor neuron and identified all of its numerous presynaptic partners. The thorough reconstruction of individual synapses in combination with functional data enabled a quantitative analysis that revealed spatial clustering of synapses from functionally synchronized cell assemblies. All of our data is publicly available.

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Section: Discussionsupporting

confidence: 89%

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Ashaber

Tomina

Kassraian-Fard

et al. 2020

Preprint

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“…Bhatla (2014) found conditioning only when the CS and US co-occurred, so conditioning in this groups may be conditional sensitization. No UAL has been found in aplysiid mollusks (Marinesco et al, 2003; Hoover et al, 2006), flat worms (Jacobson et al, 1967; Nicolas et al, 2008; Prados et al, 2013) or annelids (Crisp and Burrell, 2009; Shain, 2009). In echinoderms elemental (limited) conditioning has been reported but the necessary controls for distinguishing AL from sensitization were not performed (McClintock and Lawrence, 1982).…”

Section: Unlimited Associative Learning Its Functional Architecturesmentioning

confidence: 99%

The Transition to Minimal Consciousness through the Evolution of Associative Learning

2016

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The minimal state of consciousness is sentience. This includes any phenomenal sensory experience – exteroceptive, such as vision and olfaction; interoceptive, such as pain and hunger; or proprioceptive, such as the sense of bodily position and movement. We propose unlimited associative learning (UAL) as the marker of the evolutionary transition to minimal consciousness (or sentience), its phylogenetically earliest sustainable manifestation and the driver of its evolution. We define and describe UAL at the behavioral and functional level and argue that the structural-anatomical implementations of this mode of learning in different taxa entail subjective feelings (sentience). We end with a discussion of the implications of our proposal for the distribution of consciousness in the animal kingdom, suggesting testable predictions, and revisiting the ongoing debate about the function of minimal consciousness in light of our approach.

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“…The T cell is a low-threshold mechanosensitive neuron with input to a number of neurons that mediate motor withdrawal or escape behaviors, while the S cell is thought to be important for learning and arousal in the leech whole-body shortening reflex (Sahley et al 1994;Modney et al 1997;Burrell et al 2003;Kristan et al 2005;Crisp and Burrell 2008). The T to S synaptic circuit (Fig.…”

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confidence: 99%

Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

Li¹,

Burrell²

2011

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Persistent, bidirectional changes in synaptic signaling (that is, potentiation and depression of the synapse) can be induced by the precise timing of individual pre-and postsynaptic action potentials. However, far less attention has been paid to the ability of paired trains of action potentials to elicit persistent potentiation or depression. We examined plasticity following the pairing of spike trains in the touch mechanosensory neuron (T cell) and S interneuron (S cell) in the medicinal leech. Long-term potentiation (LTP) of T to S signaling was elicited when the T-cell spike train preceded the S-cell train. An interval 0 to +1 sec between the T-and S-cell spike trains was required to elicit long-term potentiation (LTP), and this potentiation was NMDA receptor (NMDAR)-dependent. Long-term depression (LTD) was elicited when S-cell activity preceded T-cell activity and the interval between the two spike trains was 20.2 sec to 210 sec. This surprisingly broad temporal window involved two distinct cellular mechanisms; an NMDAR-mediated LTD (NMDAR-LTD) when the pairing interval was relatively brief (,21 sec) and an endocannabinoid-mediated LTD (eCB-LTD) when longer pairing intervals were used (21 to 210 sec). This eCB-LTD also required activation of a presynaptic transient receptor potential vanilloid (TRPV)-like receptor, presynaptic Ca 2+ release from intracellular stores and activation of voltage-gated Ca 2+ channels (VGCCs). These findings demonstrate that the pairing of spike trains elicits timing-dependent forms of LTP and LTD that are supported by a complex set of cellular mechanisms involving NMDARs and endocannabinoid activation of TRPV-like receptors.[Supplemental material is available for this article.]Associative forms of long-term neuroplasticity, as first proposed by Hebb (1949), depend on the temporal relationship between pre-and postsynaptic activity. Studies of spike-timing-dependent plasticity (STDP) have provided experimental confirmation of this principle, specifically that in most connections long-term potentiation (LTP) is produced when a presynaptic action potential (or spike) precedes the postsynaptic spike, whereas long-term depression (LTD) is produced when the order is reversed (see review by Caporale and Dan 2008). In addition to the temporal order being important in determining the sign of the synaptic change, temporal proximity is also critical in that the time between the pre-and postsynaptic activity must be sufficiently brief, usually ,40 msec, to support potentiation or depression.It has been noted that the time intervals between pre-and postsynaptic activity that support STDP are not as long as those observed in many associative learning experiments, in which interstimulus intervals on the scale of seconds can be used to elicit successful conditioning (Drew and Abbott 2006). Most studies of STDP involve pairing single pre-and postsynaptic spikes or brief bursts of two to three spikes; however, many neurons communicate using relatively long trains of action potentials that are tens...

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Cellular and Behavioral Properties of Learning in Leech and Other Annelids

Cited by 9 publications

References 129 publications

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

The Transition to Minimal Consciousness through the Evolution of Associative Learning

Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms

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