Limited evidence for learning in a shuttle box paradigm in crickets (Acheta domesticus)

Aversive learning has been studied in a variety of species, such as honey bees, mice, and non-human primates. Since aversive learning has been found in some invertebrates and mammals, it will be interesting to know if this ability is shared with crickets. This paper provides data on aversive learning in male and female house crickets (Acheta domesticus) using a shuttle box apparatus. Crickets are an ideal subject for these experiments due to their well-documented learning abilities in other contexts and their readily quantifiable behaviors. The shuttle box involves a two-compartment shock grid in which a ‘master’ cricket can learn to avoid the shock by moving to specific designated locations, while a paired yoked cricket is shocked regardless of its location and therefore cannot learn. Baseline control crickets were placed in the same device as the experimental crickets but did not receive a shock. Male and female master crickets demonstrated some aversive learning, as indicated by spending more time than expected by chance in the correct (no shock) location during some parts of the experiment, although there was high variability in performance. These results suggest that there is limited evidence that the house crickets in this experiment learned how to avoid the shock. Further research with additional stimuli and other cricket species should be conducted to determine if house crickets and other species of crickets exhibit aversive learning.

Combination of successor representation-based appetitive learning and individual representation-based aversive learning is a good strategy and can be implemented in the cortico-basal ganglia circuits

While positive reward prediction errors (RPEs) and negative RPEs have equal impacts in the standard reinforcement learning, the brain appears to have distinct neural pathways for learning mainly from either positive or negative feedbacks, such as the direct and indirect pathways of the basal ganglia (BG). Given that distinct pathways may receive inputs unevenly from different neural populations and/or regions, how states or actions are represented can differ between the pathways. We explored whether combined use of different representations, coupled with different learning rates from positive and negative RPEs, has computational benefits. We considered an agent equipped with two learning systems, each of which adopted individual representation (IR) or successor representation (SR) of states. With varying the combination of IR or SR and also the learning rates from positive and negative RPEs in each system, we examined how the agent performed in a certain dynamic reward environment. We found that combination of SR-based system learning mainly from positive RPEs and IR-based system learning mainly from negative RPEs outperformed the other combinations, including IR-only or SR-only cases and the cases where the two systems had the same ratios of positive- and negative-RPE-based learning rates. In the best combination case, both systems show activities of comparable magnitudes with opposite signs, consistent with suggested profiles of BG pathways. These results suggest that particularly combining different representations with appetitive and aversive learning could be an effective learning strategy in a certain dynamic reward environment, and it might actually be implemented in the cortico-BG circuits.

Midbrain dopaminergic innervation of the hippocampus is sufficient to modulate formation of aversive memories

Aversive memories are important for survival, and dopaminergic signaling in the hippocampus has been implicated in aversive learning. However, the source and mode of action of hippocampal dopamine remain controversial. Here, we utilize anterograde and retrograde viral tracing methods to label midbrain dopaminergic projections to the dorsal hippocampus. We identify a population of midbrain dopaminergic neurons near the border of the substantia nigra pars compacta and the lateral ventral tegmental area that sends direct projections to the dorsal hippocampus. Using optogenetic manipulations and mutant mice to control dopamine transmission in the hippocampus, we show that midbrain dopamine potently modulates aversive memory formation during encoding of contextual fear. Moreover, we demonstrate that dopaminergic transmission in the dorsal CA1 is required for the acquisition of contextual fear memories, and that this acquisition is sustained in the absence of catecholamine release from noradrenergic terminals. Our findings identify a cluster of midbrain dopamine neurons that innervate the hippocampus and show that the midbrain dopamine neuromodulation in the dorsal hippocampus is sufficient to maintain aversive memory formation.

Functional organization of the midbrain periaqueductal gray for regulating aversive memory formation

Innately aversive experiences produce rapid defensive responses and powerful emotional memories. The midbrain periaqueductal gray (PAG) drives defensive behaviors through projections to brainstem motor control centers, but the PAG has also been implicated in aversive learning, receives information from aversive-signaling sensory systems and sends ascending projections to the thalamus as well as other forebrain structures which could control learning and memory. Here we sought to identify PAG subregions and cell types which instruct memory formation in response to aversive events. We found that optogenetic inhibition of neurons in the dorsolateral subregion of the PAG (dlPAG), but not the ventrolateral PAG (vlPAG), during an aversive event reduced memory formation. Furthermore, inhibition of a specific population of thalamus projecting dlPAG neurons projecting to the anterior paraventricular thalamus (aPVT) reduced aversive learning, but had no effect on the expression of previously learned defensive behaviors. By contrast, inactivation of dlPAG neurons which project to the posterior PVT (pPVT) or centromedial intralaminar thalamic nucleus (CM) had no effect on learning. These results reveal specific subregions and cell types within PAG responsible for its learning related functions.

Associative learning and memory through metamorphosis in Grapholita molesta (Busck) (Lepidoptera: Tortricidae)

Learning of chemical stimuli by insects can occur during the larval or adult life stage, resulting in changes in the imago chemotaxic behaviour. There is little information on learning in Tortricidae, and associative learning through metamorphosis is unknown in this group. Here, we evaluate the influence of olfactory aversive learning in Grapholita molesta (Busck) (Lepidoptera: Tortricidae) during the immature stage and determine if memory persists after metamorphosis. Larvae (10–12 days old) were conditioned to associate the odour of ethyl acetate with pulses of aversive electric shock. Insects were exposed to air, to the ethyl acetate odour, and to shock, in isolation or combination. After conditioning, both larvae and adults were tested in a two-choice olfactometer. Larvae exposed only to air or ethyl acetate increased legibility. Larvae trained with ethyl acetate and shock simultaneously exhibited significant avoidance to ethyl acetate. Avoidance was still present for at least 72 hours after metamorphosis. Thus, G. molesta has the ability to associate an odour to an aversive stimulus precociously, and this association is maintained through metamorphosis and persists into adulthood.