Where is the trace in trace conditioning?

Woodruff-Pak, Diana S.; Disterhoft, John F.

doi:10.1016/j.tins.2007.11.006

Cited by 170 publications

(153 citation statements)

References 74 publications

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“…Evidence is accumulating in mammals concerning the involvement of different brain systems (3). Here, we characterized trace conditioning in the fruit fly and used mutant analyses to show that it is distinct from the well-characterized simultaneous conditioning at the molecular level.…”

Section: Discussionmentioning

confidence: 99%

Distinct molecular underpinnings of Drosophila olfactory trace conditioning

Shuai

Qin

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Trace conditioning is valued as a simple experimental model to assess how the brain associates events that are discrete in time. Here, we adapted an olfactory trace conditioning procedure in Drosophila melanogaster by training fruit flies to avoid an odor that is followed by foot shock many seconds later. The molecular underpinnings of the learning are distinct from the well-characterized simultaneous conditioning, where odor and punishment temporally overlap. First, Rutabaga adenylyl cyclase (Rut-AC), a putative molecular coincidence detector vital for simultaneous conditioning, is dispensable in trace conditioning. Second, dominant-negative Rac expression, thought to sustain early labile memory, significantly enhances learning of trace conditioning, but leaves simultaneous conditioning unaffected. We further show that targeting Rac inhibition to the mushroom body (MB) but not the antennal lobe (AL) suffices to achieve the enhancement effect. Moreover, the absence of trace conditioning learning in D1 dopamine receptor mutants is rescued by restoration of expression specifically in the adult MB. These results suggest the MB as a crucial neuroanatomical locus for trace conditioning, which may harbor a Rac activity-sensitive olfactory "sensory buffer" that later converges with the punishment signal carried by dopamine signaling. The distinct molecular signature of trace conditioning revealed here shall contribute to the understanding of how the brain overcomes a temporal gap in potentially related events.learning and memory | olfaction | cAMP | Rho GTPase I n trace conditioning, the conditional stimulus (CS) and the unconditional stimulus (US) are separated in time by a stimulus-free interval (1). This so-called "trace interval" can last for a fraction of a second in eyeblink conditioning but many seconds in fear conditioning, which poses a challenging question: how does the brain overcome this temporal gap to form the association between the CS and US (2)? Intriguingly, trace conditioning in mammals engages neural substrates fundamentally different from delay conditioning, where the CS precedes but also temporally overlaps with the US (3). Early evidence comes from lesion studies with experimental animals showing that acquisition of trace conditioning requires intact hippocampal formation (4, 5) and medial prefrontal cortex (6), whereas delay conditioning can occur even with the entire forebrain removed (7,8). Later studies involving human subjects further validate the involvement of different brain circuits in these two conditioning variants and even suggest, more surprisingly, that conscious awareness might be a prerequisite for trace but not delay conditioning (9, 10). It is then hypothesized that the participation of hippocampus and neocortex, as well as the associated higher cognitive function, is necessary in trace conditioning to maintain a representation of the CS or CS/US contingency so as to bridge the temporal gap (11, 12). However, little is known about what form this representation takes and how it e...

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Section: Discussionmentioning

confidence: 99%

Distinct molecular underpinnings of Drosophila olfactory trace conditioning

Shuai

Qin

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Thus, generalization can be used as a tool to measure the perceived quality of a CS in relation to other test odors. If trace and delay conditioning engage different brain areas, as is the case in mammals (Woodruff-Pak and Disterhoft, 2008), one would expect differences in the perceived odor quality between trace and delay conditioning, because neural odor representations change over time (Galán et al, 2004) and along different processing levels of the olfactory pathway (Linster et al, 2005;Szyszka et al, 2005). We therefore asked whether the perceived odor quality differs between trace memory and delay conditioning (Fig.…”

Section: Trace and Delay Conditioning Share Basic Propertiesmentioning

confidence: 99%

“…Perhaps the most striking difference to mammalian trace conditioning is that honeybees acquire odor trace memories during a single learning trial (Fig. 3Aii), whereas trace eyeblink conditioning requires several hundred training trials (Woodruff-Pak and Disterhoft, 2008). Honeybees' ability to acquire a trace memory after only a single trial requires the existence of a US-independent CS trace.…”

Section: Single-trial Acquisition Reveals a Sensory Odor Tracementioning

confidence: 99%

Mind the Gap: Olfactory Trace Conditioning in Honeybees

Szyszka¹,

Demmler²,

Oemisch³

et al. 2011

J. Neurosci.

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Trace conditioning is a form of classical conditioning, where a neutral stimulus (conditioned stimulus, CS) is associated with a following appetitive or aversive stimulus (unconditioned stimulus, US). Unlike classical delay conditioning, in trace conditioning there is a stimulus-free gap between CS and US, and thus a poststimulus neural representation (trace) of the CS is required to bridge the gap until its association with the US. The properties of such stimulus traces are not well understood, nor are their underlying physiological mechanisms. Using behavioral and physiological approaches, we studied appetitive olfactory trace conditioning in honeybees. We found that single-odor presentation created a trace containing information about odor identity. This trace conveyed odor information about the initial stimulus and was robust against interference by other odors. Memory acquisition decreased with increasing CS-US gap length. The maximum learnable CS-US gap length could be extended by previous trace-conditioning experience. Furthermore, acquisition improved when an additional odor was presented during the CS-US gap. Using calcium imaging, we tested whether projection neurons in the primary olfactory brain area, the antennal lobe, contain a CS trace. We found odor-specific persistent responses after stimulus offset. These post-odor responses, however, did not encode the CS trace, and perceived odor quality could be predicted by the initial but not by the post-odor response. Our data suggest that olfactory trace conditioning is a less reflexive form of learning than classical delay conditioning, indicating that odor traces might involve higher-level cognitive processes.

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“…Classical conditioning of the eyeblink response serves as an excellent model in which to investigate the mechanisms of associative learning and memory in mammals [2][3][4][5][6][7][8][9] . In this paradigm, a conditioned stimulus (CS; e.g., a tone or light) is followed by an unconditioned stimulus (US; e.g., a corneal air-puff or periorbital shock).…”

Section: Introductionmentioning

confidence: 99%

“…Instead, with repeated there is a temporal gap between the CS and the US and they terminate together [9,10] . The view is widely held that TEC is dependent on awareness [11][12][13][14] .…”

Section: Introductionmentioning

confidence: 99%

Awareness is essential for differential delay eyeblink conditioning with soft-tone but not loud-tone conditioned stimuli

Huang

et al. 2014

Neurosci. Bull.

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The role of awareness in differential delay eyeblink conditioning (DEC) remains controversial. Here, we investigated the involvement of awareness in differential DEC with a soft or a loud tone as the conditioned stimulus (CS). In the experiment, 36 participants were trained in differential DEC with a soft tone (60 dB) or a loud tone (85 dB) as the CS, paired with a corneal air-puff as the unconditioned stimulus (US). After conditioning, awareness of the relationship between the CS and the US was assessed with a 17-item true/false questionnaire. Interestingly, during differential DEC with a soft-tone CS, a higher proportion of differential conditioned responses (CRs) was evident in participants who were aware than those who were unaware. In contrast, when a loud tone was used as the CS, the proportion of differential CRs of the aware participants did not differ signifi cantly from those who were unaware over any of the blocks of 20 trials. In unaware participants, the percentage of differential CRs with a loud-tone CS was significantly higher than that with a soft-tone CS; however in participants classified as aware, the percentage of differential CRs with a loud-tone CS did not differ significantly from that with a soft-tone CS. The present findings suggest that awareness is critical for differential DEC when the delay task is rendered more diffi cult.

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Where is the trace in trace conditioning?

Cited by 170 publications

References 74 publications

Distinct molecular underpinnings of Drosophila olfactory trace conditioning

Distinct molecular underpinnings of Drosophila olfactory trace conditioning

Mind the Gap: Olfactory Trace Conditioning in Honeybees

Awareness is essential for differential delay eyeblink conditioning with soft-tone but not loud-tone conditioned stimuli

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