Is Novelty Detection Important in Long-Term Odor Memory?

Memory for odors is believed to be longer-lasting than memory for visual stimuli, as is evidenced by flat forgetting curves. However, performance on memory tasks is typically weaker in olfaction than vision. Studies of odor memory that use forced-choice methods confound responses that are a result of a trace memory and responses that can be obtained through process of elimination. Moreover, odor memory is typically measured with common stimuli, which are more familiar and responses may be confounded by verbal memory, and measure memory in intentional learning conditions, which are ecologically questionable. Here we demonstrate the value of using tests of memory in which hit rate and correct rejection rate are evaluated separately (i.e., not using forced-choice methods) and uncommon stimuli are used. This study compared memory for common and uncommon odors and pictures that were learned either intentionally (Exp. 1) or incidentally (Exp. 2) and tested with either a forced-choice or a one-stimulus-at-a-time (“monadic”) recognition task after delays of 15 min, 48 h or 1 week. As expected, memory declined with delay in most conditions, but depended upon the particular measure of memory and was better for pictures than odors and for common than uncommon stimuli. For common odors, hit rates decreased with delay but correct rejection rates remained constant with delay. For common pictures, we found the opposite result, constant hit rates and decreased correct rejection rates. Our results support the ‘misfit theory of conscious olfactory perception’, which highlights the importance of the detection of novelty in olfactory memory and suggests that olfactory memory should be studied using more ecologically valid methods.

Interneuron activity-structural plasticity association is driven by context-dependent sensory experience

Neuronal dendritic spine dynamics provide a plasticity mechanism for altering brain circuit connectivity to integrate new information for learning and memory. Previous in vivo studies in the olfactory bulb (OB) showed that regional increases in activity caused localized spine stability, at a population level, yet how activity affects spine dynamics at an individual neuron level remains unknown. In this study, we tracked in vivo the correlation between an individual neuron’s activity and its dendritic spine dynamics of OB granule cell (GC) interneurons. Odor experience caused a consistent correlation between individual GC activity and spine stability. Dissecting the components of the OB circuit showed that increased principal cell (MC) activity was sufficient to drive this correlation, whereas cell-autonomously driven GC activity had no effect. A mathematical model was able to replicate the GC activity-spine stability correlation and showed MC output having improved odor discriminability while retaining odor memory. These results reveal that GC spine plasticity provides a sufficient network mechanism to decorrelate odors and maintain a memory trace.

In-vivo evidence for proximodistal heterogeneity in hippocampal CA1 and CA3 during non-spatial memory retrieval

Recent immediate early gene evidence suggests that proximal CA3 (proxCA3, close to dentate gyrus) and distal CA1 (distCA1, close to subiculum) form a specialized non-spatial hippocampal subnetwork (nakamura et al, JON, 2013; Beer and Vavra, Plos Biology, 2018) while distal CA3 (distCA3) and proximal CA1 (proxCA1) are more specialized in spatial information processing (Flashbeck et al, 2018). However, direct in-vivo evidence for such functional networks are still missing. Here, we used chronically implanted multi-tetrode recording technique to simultaneously record along the proximodistal axis of the two CA-fields while rats performed a high-demanding delayed non-match to odor memory task. In this task, rats smelled 10 (old) odors during the study phase, and after a 20-minute delay memory for the studied odors was tested by exposing rats to the same odors intermixed with 10 new odors. We recorded 193 CA3- and 367 CA1-neurons in 5 animals who could perfom above threshold (75%). Using Support Vector Machine (SVM) we tested whether proxCA3-distCA1 neurons (non-spatial network) can differentiate the old from new odors better than distCA3-proxCA1 neurons (spatial network). We found that activity in the proxCA3-distCA1 network was relevant for the discrimination between old from new odors and similar to behavior; in contrast, the activity of the distCA3-proxCA1 network was not. Further, we found a gradient in the distribution of task-relevant neurons along the transverse axis of CA1 as well as CA3. Overall, we provide clear in vivo electrophysiological evidence that supports the role of proxCA3-distCA1 network in non-spatial memory processing.

Odor, Memory, and Proust

Chapter 8, “Odor, Memory, and Proust,” draws together the previous themes of emotion and language and relates them to memory. The chapter begins by examining some evidence from the psychology of autobiographical memory concerning voluntary and involuntary memory and its relation to age. The second part of the chapter discusses psychologists’ use and misuse of the Proustian type of involuntary memory, exploring the way Proust at the end of Remembrance of Things Past expounds his idea of sensory epiphanies, which are signs of transcendence and many of which involve smell. The chapter ends by contrasting the Proustian literary epiphanies with the directness of two Holocaust memoirs that bring horrendous smell experiences to expression with a vividness that shows one need not be a literary professional in order to express smell convincingly in language.

Regulation of olfactory associative memory by the circadian clock output signal Pigment-dispersing factor (PDF)

ABSTRACTDissociation between the output of the circadian clock and external environmental cues is a major cause of human cognitive dysfunction. While the effects of ablation of the molecular clock on memory have been studied in many systems, little has been done to test the role of specific clock circuit output signals. To address this gap, we examined the effects of mutation of Pigment-dispersing factor (Pdf) and its receptor, Pdfr on associative memory in male and female Drosophila. Loss of PDF signaling significantly decreases the ability to form associative memory. Appetitive short-term memory (STM), which in wildtype is time-of-day (TOD)-independent, is decreased across the day by mutation of Pdf or Pdfr, but more substantially in the morning than in the evening. This defect is due to PDFR expression in adult neurons outside the core clock circuit and the mushroom body Kenyon cells. The acquisition of a TOD difference in mutants implies the existence of multiple oscillators that act to normalize memory formation across the day for appetitive processes. Interestingly, aversive STM requires PDF but not PDFR, suggesting that there are valence-specific pathways downstream of PDF that regulate memory formation. These data argue that the circadian clock uses circuit-specific and molecularly diverse output pathways to enhance the ability of animals to optimize responses to changing conditions.SIGNIFICANCE STATEMENTFrom humans to invertebrates, cognitive processes are influenced by organisms’ internal circadian clocks, the pace of which is linked to the solar cycle. Disruption of this link is increasingly common (e.g. jetlag, social jetlag disorders) and causes cognitive impairments that are costly and long-lasting. A detailed understanding of how the internal clock regulates cognition is critical for the development of therapeutic methods. Here, we show for the first time that olfactory associative memory in Drosophila requires signaling by Pigment-dispersing factor (PDF), a neuromodulatory signaling peptide produced only by circadian clock circuit neurons. We also find a novel role for the clock circuit in stabilizing appetitive sucrose/odor memory across the day.