Sensory Memory for Odors Is Encoded in Spontaneous Correlated Activity Between Olfactory Glomeruli

Sensory memory is a short-lived persistence of a sensory stimulus in the nervous system, such as iconic memory in the visual system. However, little is known about the mechanisms underlying olfactory sensory memory. We have therefore analyzed the effect of odor stimuli on the first odor-processing network in the honeybee brain, the antennal lobe, which corresponds to the vertebrate olfactory bulb. We stained output neurons with a calcium-sensitive dye and measured across-glomerular patterns of spontaneous activity before and after a stimulus. Such a single-odor presentation changed the relative timing of spontaneous activity across glomeruli in accordance with Hebb's theory of learning. Moreover, during the first few minutes after odor presentation, correlations between the spontaneous activity fluctuations suffice to reconstruct the stimulus. As spontaneous activity is ubiquitous in the brain, modifiable fluctuations could provide an ideal substrate for Hebbian reverberations and sensory memory in other neural systems.

[1]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[2]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[3]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

[4]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[5]  G. Laurent,et al.  Short-term memory in olfactory network dynamics , 1999, Nature.

[6]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[7]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[8]  M. Elphick,et al.  Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo‐tactile centers argue against a generic role in sensory integration , 2007, The Journal of comparative neurology.

[9]  S. Grillner,et al.  Microcircuits : the interface between neurons and global brain function , 2006 .

[10]  C. Giovanni Galizia,et al.  Odor-Driven Attractor Dynamics in the Antennal Lobe Allow for Simple and Rapid Olfactory Pattern Classification , 2004, Neural Computation.

[11]  Martin Beckerman Adaptive Cooperative Systems , 1997 .

[12]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[13]  A Borst,et al.  Spatial distribution and characteristics of voltage-gated calcium signals within visual interneurons. , 2000, Journal of neurophysiology.

[14]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[15]  Randolf Menzel,et al.  Odour perception in honeybees: coding information in glomerular patterns , 2000, Current Opinion in Neurobiology.

[16]  Menzel,et al.  The role of glomeruli in the neural representation of odours: results from optical recording studies. , 2001, Journal of insect physiology.

[17]  T. Christensen,et al.  Functional Characteristics of the Antennal Lobe , 1999 .

[18]  Donald A Wilson,et al.  Olfactory Bulb Mitral-Tufted Cell Plasticity: Odorant-Specific Tuning Reflects Previous Odorant Exposure , 2003, The Journal of Neuroscience.

[19]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[20]  Jerry Ray Dias,et al.  Chaotic itinerancy, temporal segmentation and spatio-temporal combinatorial codes , 2006, Physica D: Nonlinear Phenomena.

[21]  M. Srinivasan,et al.  The concepts of ‘sameness’ and ‘difference’ in an insect , 2001, Nature.

[22]  William H. Press,et al.  Numerical recipes in C , 2002 .

[23]  Daniel Flanagan,et al.  Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybeeApis mellifera , 1989, Journal of Comparative Physiology A.

[24]  Randolf Menzel,et al.  A semi-in-vivo preparation for optical recording of the insect brain , 1997, Journal of Neuroscience Methods.

[25]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

[26]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[27]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[28]  R. Menzel,et al.  Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. , 2002, Journal of Comparative Physiology A.

[29]  Gianluigi Mongillo,et al.  Selective delay activity in the cortex: phenomena and interpretation. , 2003, Cerebral cortex.

[30]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[31]  R. Clark,et al.  Classical conditioning, awareness, and brain systems , 2002, Trends in Cognitive Sciences.

[32]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

[33]  X. Sun,et al.  Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours , 1993 .

[34]  S. Sachse,et al.  Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. , 2002, Journal of neurophysiology.

[35]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[36]  R. Menzel,et al.  The glomerular code for odor representation is species specific in the honeybee Apis mellifera , 1999, Nature Neuroscience.

[37]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[38]  B. Kimmerle,et al.  Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy , 2003, Journal of Comparative Physiology A.

[39]  R. Menzel,et al.  A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy , 1999, Cell and Tissue Research.

[40]  Lars Chittka,et al.  Recognition of flowers by pollinators. , 2006, Current opinion in plant biology.

[41]  W. Getz,et al.  Honeybee olfactory sensilla behave as integrated processing units. , 1994, Behavioral and neural biology.

[42]  Silke Sachse,et al.  Topography and Dynamics of the Olfactory System , 2006 .

[43]  P. D. Giudice,et al.  Modelling the formation of working memory with networks of integrate-and-fire neurons connected by plastic synapses , 2003, Journal of Physiology-Paris.

[44]  S. Korsching Olfactory maps and odor images , 2002, Current Opinion in Neurobiology.

[45]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.