Storing maternal memories: hypothesizing an interaction of experience and estrogen on sensory cortical plasticity to learn infant cues

Abstract

Much of the literature on maternal behavior has focused on the role of infant experience and hormones in a canonical subcortical circuit for maternal motivation and maternal memory. Although early studies demonstrated that the cerebral cortex also plays a significant role in maternal behaviors, little has been done to explore what that role may be. Recent work though has provided evidence that the cortex, particularly sensory cortices, contains correlates of sensory memories of infant cues, consistent with classical studies of experience-dependent sensory cortical plasticity in non-maternal paradigms. By reviewing the literature from both the maternal behavior and sensory cortical plasticity fields, focusing on the auditory modality, we hypothesize that maternal hormones (predominantly estrogen) may act to prime auditory cortical neurons for a longer-lasting neural trace of infant vocal cues, thereby facilitating recognition and discrimination. This couldthen more efficiently activate the subcortical circuit to elicit and sustain maternal behavior.

Keywords: Auditory cortex; Estradiol; Estrogen; Experience-dependent plasticity; Infant; Maternal behavior; Memory; Natural stimulus; Parenting; Vocalization.

Figure 1

Example spectrogram of a USV bout from an individual postnatal day 7 mouse pup. Darker colors correspond to higher intensities in the sound signal at corresponding frequencies. These calls concentrate in the 60-80 kHz range, and feature moderate frequency modulation, as well as temporal structure in the form of a ~5 Hz repetition rate, which for comparison, is comparable to the typical syllable rate in human speech.

Figure 2

Schematic of the neural pathways for olfactory and auditory cues from pups to reach the canonical subcortical maternal circuit based on the Numan model (Numan, 2007). Small arrows indicate predominantly excitatory connections; bars indicate presumed inhibitory connections; open triangles indicate neuromodulatory inputs. For clarity, not all connections are shown in order to concentrate on those that form the basis of our knowledge about the information flow, especially for auditory cues, which is the focus of this review. Auditory cortex is a key site for experience-dependent sensory plasticity, thought to be guided by neuromodulatory inputs from the dopaminergic, cholinergic, noradrenergic and other systems. Changes in the neural representation of pup vocalizations can be conveyed into the maternal circuit through limbic as well as prefrontal pathways, potentially modulating the drive for maternal responsiveness.

Figure 3

Parallel effects for maternal hormones and pup experience on consolidation of maternal responsiveness and pup call recognition. Consolidation of maternal responsiveness is measured by the latency (in days) to express consistent maternal care for live pups weeks after an initial exposure to pups (or hormone treatment in the absence of pup experience). Without that exposure, or if that exposure is brief and occurs without maternal levels of hormones, the latency to express maternal behaviors on the retest is generally slow (i.e. longer than 3 days). However, in the presence of maternal hormones, an initial pup exposure as short as 30 minutes facilitates more rapid reinstatement of maternal care more than a week later. This pattern is mirrored for pup call recognition, which is measured in a two-alternative choice phonotaxis task between the playback of calls or a neutral sound. Artificially raising estradiol (E2) and progesterone (P) to maternal levels without exposure to pups is insufficient to acquire call recognition, as is brief exposure without hormones. Longer exposure without maternal hormones can be effective for establishing call recognition, but it is not maintained for the long-term, when tested a month later. The combination of maternal hormones during pup exposure appears sufficient to establish and maintain call recognition up to a month after weaning.

Figure 4

Schematic illustration of improved neural population contrast across auditory cortex in mothers for pup USVs. Call-evoked excitation is similar between mothers and pup-naïve virgins, with generally stronger (darker shade of red) excitatory responses in the ultrasound field, UF. Call-evoked inhibition is similar in UF between mothers and virgins, but stronger (darker shade of blue) in mothers for the lateral band core auditory cortical fields, A1 and AAF. Assuming downstream sites pool call-excitatory and inhibitory responses together, these patterns would produce a stronger contrast in activity between UF versus A1/AAF for mothers compared to virgins.