Short-Term Plasticity Regulates Both Divisive Normalization and Adaptive Responses in Drosophila Olfactory System

In Drosophila, olfactory information received by olfactory receptor neurons (ORNs) is first processed by an incoherent feed forward neural circuit in the antennal lobe (AL) that consists of ORNs (input), inhibitory local neurons (LNs), and projection neurons (PNs). This “early” olfactory information processing has two important characteristics. First, response of a PN to its cognate ORN is normalized by the overall activity of other ORNs, a phenomenon termed “divisive normalization.” Second, PNs respond strongly to the onset of ORN activities, but they adapt to prolonged or continuously varying inputs. Despite the importance of these characteristics for learning and memory, their underlying mechanisms are not fully understood. Here, we develop a circuit model for describing the ORN-LN-PN dynamics by including key neuron-neuron interactions such as short-term plasticity (STP) and presynaptic inhibition (PI). By fitting our model to experimental data quantitatively, we show that a strong STP balanced between short-term facilitation (STF) and short-term depression (STD) is responsible for the observed nonlinear divisive normalization in Drosophila. Our circuit model suggests that either STP or PI alone can lead to adaptive response. However, by comparing our model results with experimental data, we find that both STP and PI work together to achieve a strong and robust adaptive response. Our model not only helps reveal the mechanisms underlying two main characteristics of the early olfactory process, it can also be used to predict PN responses to arbitrary time-dependent signals and to infer microscopic properties of the circuit (such as the strengths of STF and STD) from the measured input-output relation. Our circuit model may be useful for understanding the role of STP in other sensory systems.

Exploring the Role of Cognition in the Annual Fall Migration of the Monarch Butterfly (Danaus plexippus)

Each fall, monarch butterflies in eastern North America undergo an extraordinary long-distance migration to wintering areas in central Mexico, where they remain until returning northward in the spring. Migrants survive the overwintering period by metabolizing lipid reserves accumulated exclusively though floral nectar; however, there is little known about how individuals maximize foraging efficiency in the face of floral environments that constantly change in complex and unpredictable ways along their migratory route. Here, a proboscis extension paradigm is used to investigate the role of cognition during the foraging phase of monarch migration. Male and female migratory butterflies were consecutively trained to discriminate between two color and odor cues and then tested for their ability to simultaneously retain the information on the reward value of each cue in memory without reinforcement over a period of 7 days. To gain further insight into cognitive abilities of monarchs as a migratory species, a second set of captive-reared males and females were tested under harnessed conditions at the same time as wild-caught fall migrants. Results showed that male and female migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies, as a migratory species, have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation.

Smell of green leaf volatiles attracts white storks to freshly cut meadows

Finding food is perhaps the most important task for all animals. Birds often show up unexpectedly at novel food sources such as freshly tilled fields or mown meadows. Here we test whether wild European white storks primarily use visual, social, auditory or olfactory information to find freshly cut farm pastures where insects and rodents abound. Aerial observations of an entire local stork population documented that birds could not have become aware of a mown field through auditory, visual or social information. Only birds within a 75° downwind cone over 0.4–16.6 km approached any mown field. Placing freshly cut grass from elsewhere on selected unmown fields elicited similarly immediate stork approaches. Furthermore, uncut fields that were sprayed with a green leaf volatile organic compound mix ((Z)-3-hexenal, (Z)-3-hexenol, hexenyl acetate), the smell of freshly cut grass, immediately attracted storks. The use of long-distance olfactory information for finding food may be common in birds, contrary to current perception.

Effects of short-term plasticity in early olfactory information processing in Drosophila

In Drosophila, olfactory information received by the olfactory receptor neurons (ORNs) is first processed by an incoherent feed forward neural circuit in the antennal lobe (AL) that consists of ORNs (input), the inhibitory local neurons (LNs), and projection neurons (PNs). This "early" olfactory information process has two important characteristics. First, response of a PN to its cognate ORN is normalized by the overall activity of other ORNs, a phenomenon termed "divisive normalization". Second, PNs respond strongly to the onset of ORN activities, but they adapt to prolonged or continuously increasing inputs. Despite the importance of these characteristics for learning and memory, their underlying mechanism remains not fully understood. Here, we develop a circuit model for describing the ORN-LN-PN dynamics by including key features of neuron-neuron interactions, in particular short-term plasticity (STP) and presynaptic inhibition (PI).Our model shows that STP is critical in shaping PN's steady-state response properties. By fitting our model to experimental data quantitatively, we found that strong and balanced short-term facilitation (STF) and short-term depression (STD) in STP is crucial for the observed nonlinear divisive normalization in Drosophila. By comparing our model with the observed adaptive response to time-varying signals quantitatively, we find that both STP and PI contribute to the highly adaptive response with the latter being the dominant factor for a better fit with experimental data. Our model not only helps reveal the mechanisms underlying two main characteristics of the early olfactory process, it can also be used to predict the PN responses to arbitrary time-dependent signals and to infer microscopic properties of the circuit (such as the strengths of STF and STD) from the measured input-output relation.

Ongoing habenular activity is driven by forebrain networks and modulated by olfactory stimuli

SUMMARYOngoing neural activity, which represents internal brain states, is constantly modulated by the sensory information that is generated by the environment. In this study, we show that the habenular circuits act as a major brain hub integrating the structured ongoing activity of the limbic forebrain circuitry and the olfactory information. We demonstrate that ancestral homologs of amygdala and hippocampus in zebrafish forebrain are the major drivers of ongoing habenular activity. We also reveal that odor stimuli can modulate the activity of specific habenular neurons that are driven by this forebrain circuitry. Our results highlight a major role for the olfactory system in regulating the ongoing activity of the habenula and the forebrain, thereby altering brain’s internal states.

The smell of cooperation: rats increase helpful behaviour when receiving odour cues of a conspecific performing a cooperative task

Reciprocity can explain cooperative behaviour among non-kin, where individuals help others depending on their experience in previous interactions. Norway rats ( Rattus norvegicus ) cooperate reciprocally according to direct and generalized reciprocity. In a sequence of four consecutive experiments, we show that odour cues from a cooperating conspecific are sufficient to induce the altruistic help of rats in a food-exchange task. When rats were enabled to help a non-cooperative partner while receiving olfactory information from a rat helping a conspecific in a different room, they helped their non-cooperative partner as if it was a cooperative one. We further show that the cues inducing altruistic behaviour are released during the act of cooperation and do not depend on the identity of the cue provider. Remarkably, olfactory cues seem to be more important for cooperation decisions than experiencing a cooperative act per se . This suggests that rats may signal their cooperation propensity to social partners, which increases their chances to receive help in return.

Encoding of odor information and reward anticipation in anterior cortical amygdaloid nucleus

Olfactory information directly reaches the amygdala through the olfactory cortex, without the involvement of thalamic areas, unlike other sensory systems. The anterior cortical amygdaloid nucleus (ACo) is one of the olfactory cortices that receives olfactory sensory input, and is part of the olfactory cortical amygdala, which relays olfactory information to the amygdala. To examine its electrophysiological features, we recorded individual ACo neurons during the odor-guided go/no-go task to obtain a water reward. Many ACo neurons exhibited odor-evoked go cue-preferred during the late phase of odor-sampling supporting the population dynamics that differentiate go/no-go responses before executing the odor-evoked behaviors. We observed two types of neurons with different anticipation signals: one neuron type exhibited gradual increases of activity toward reward delivery, while another type exhibited a phasic go cue-preferred activity during odor sampling as well as another phasic anticipatory activity for rewards. These results suggest that the ACo may be involved in reward-related behavioral learning by associating the olfactory information with reward anticipation.