Emergence of Learned Categorical Representations within an Auditory Forebrain Circuit

Abstract

Many learned behaviors are thought to require the activity of high-level neurons that represent categories of complex signals, such as familiar faces or native speech sounds. How these complex, experience-dependent neural responses emerge within the brain's circuitry is not well understood. The caudomedial mesopallium (CMM), a secondary auditory region in the songbird brain, contains neurons that respond to specific combinations of song components and respond preferentially to the songs that birds have learned to recognize. Here, we examine the transformation of these learned responses across a broader forebrain circuit that includes the caudolateral mesopallium (CLM), an auditory region that provides input to CMM. We recorded extracellular single-unit activity in CLM and CMM in European starlings trained to recognize sets of conspecific songs and compared multiple encoding properties of neurons between these regions. We find that the responses of CMM neurons are more selective between song components, convey more information about song components, and are more variable over repeated components than the responses of CLM neurons. While learning enhances neural encoding of song components in both regions, CMM neurons encode more information about the learned categories associated with songs than do CLM neurons. Collectively, these data suggest that CLM and CMM are part of a functional sensory hierarchy that is modified by learning to yield representations of natural vocal signals that are increasingly informative with respect to behavior.

Large-Scale Synchronized Activity during Vocal Deviance Detection in the Zebra Finch Auditory Forebrain

“…Site pairs have been categorized depending on whether or not the distance between them is Ͼ600 m. For most site pairs, cross-covariance is maximal at 0.0 ms. responses in CLM are distinctly different with respect to the temporal scale of stimulus history sensitivity from those in the medial parts of CMM and NCM. Some support for this hypothesis is provided by the recent finding that in starlings, Sturnus vulgaris, CMM neurons show more variable responses to repeated components of song than CLM neurons do (Jeanne et al, 2011).…”

“…Thus, the auditory scene of these birds is rife with behaviorally meaningful stimuli that recur on short timescales. Although the songbird auditory forebrain has been studied extensively in terms of acoustic feature coding (Müller and Leppelsack, 1985;Theunissen et al, 2000;Grace et al, 2003;Cousillas et al, 2005;Nagel and Doupe, 2006;Amin et al, 2007;Meliza et al, 2010;Jeanne et al, 2011), much less is known about its sensitivity to short-term history of natural stimuli. We recently found in the medial auditory forebrain widespread depression of responses to call stimuli that recur at natural rates (Beckers and Gahr, 2010), but if and how such modulation underlies the detection of unexpected calls remains unclear.…”

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

“…Learned visual associations in monkeys are reflected by association-selective representations in higher visual areas of the temporal cortex (21,22), with top-down activation by the PFC contributing to prospective representations of the choice picture to be recalled (19). Changes to stimulus-selective representations in higher sensory areas have also been reported in anesthetized starlings trained on auditory discriminations (23)(24)(25). Single neurons as well as population activity in auditory association areas contained information about the behavioral relevance of different sounds.…”

A neural basis for password-based species recognition in an avian brood parasite

“…On the other hand, the CMM in juvenile cowbirds does not exhibit differential ZENK induction in response to the chatter. It is possible that the NCM in juveniles and adults provides a neural representation of a password for species recognition, whereas discrimination tasks that require finer tuning and greater subtlety, especially with songs that require learning, may be within the domain of the CMM (Jeanne et al, 2011). Thus, juvenile birds that have less experience with song exposure or various song qualities compared with adults would express less ZENK induction in this region after exposure to chatter.…”