Seasonal plasticity in the adult somatosensory cortex

Significance To survive, animals need to adapt to changes of their ecosystem by changing their behaviors or even morphing the organs responsible for generating these behaviors. Small mammals have a high metabolic rate, and to balance energy deficits during winter they can decrease their brain and body size, a phenomenon termed Dehnel’s effect. We find specific seasonal changes in the brain of the smallest terrestrial mammal, the Etruscan shrew. Their cortex shrinks in the winter, with layer-width and neuron number reduction in the energetically expensive somatosensory cortical layer 4. Imaging of neural activity revealed reduced suppressive responses to whisker touch during winter, indicating that such cortical adaptation may have synergistic functional and behavioral effects in addition to direct metabolic benefits.
Seasonal cycles govern life on earth, from setting the time for the mating season to influencing migrations and governing physiological conditions like hibernation. The effect of such changing conditions on behavior is well-appreciated, but their impact on the brain remains virtually unknown. We investigate long-term seasonal changes in the mammalian brain, known as Dehnel’s effect, where animals exhibit plasticity in body and brain sizes to counter metabolic demands in winter. We find large seasonal variation in cellular architecture and neuronal activity in the smallest terrestrial mammal, the Etruscan shrew, Suncus etruscus. Their brain, and specifically their neocortex, shrinks in winter. Shrews are tactile hunters, and information from whiskers first reaches the somatosensory cortex layer 4, which exhibits a reduced width (−28%) in winter. Layer 4 width (+29%) and neuron number (+42%) increase the following summer. Activity patterns in the somatosensory cortex show a prominent reduction of touch-suppressed neurons in layer 4 (−55%), the most metabolically active layer. Loss of inhibitory gating occurs with a reduction in parvalbumin-positive interneurons, one of the most active neuronal subtypes and the main regulators of inhibition in layer 4. Thus, a reduction in neurons in layer 4 and particularly parvalbumin-positive interneurons may incur direct metabolic benefits. However, changes in cortical balance can also affect the threshold for detecting sensory stimuli and impact prey choice, as observed in wild shrews. Thus, seasonal neural adaptation can offer synergistic metabolic and behavioral benefits to the organism and offer insights on how neural systems show adaptive plasticity in response to ecological demands.