A singing canary

When a canary sings, it maintains a memory trace of the notes produced in the previous five to 10 seconds, a process that allows the bird to produce songs with long-range rules or syntactic structure, according to a new study co-written by a neuroscientist at the University of Oregon’s Phil and Penny Knight Campus for Accelerating Scientific Impact.

In the project, a nine-member team used tiny, head-mounted microscopes to track the activity of the output neurons that reside in a canary’s high vocal center, a brain area involved in song motor control. In prior studies, the activity of these neurons had been identified in simpler singers, revealing one of the most precise patterns of neural activity observed in any organism.

Newly applied to the more complex song of canaries, the neurons were seen activating in specific sequential contexts, with the rules of activation spanning up to 40 syllables over four seconds. The team’s paper was published online June 17 by the journal Nature.

The research opens a window on theorized “hidden states” of the brain, a form of short-term memory that integrates past information with ongoing motor control, said Tim Gardner, an associate professor and the DeArmond Chair in Neuro-Engineering in the Knight Campus.

Studying short-term motor memory in canaries provides an opportunity to examine a high-level motor phenomenon in a controlled model system, one that is akin to how studies of the hydrogen atom helped crack the code of quantum mechanics at its inception, Gardner said.

“You want to examine a new phenomenon using the simplest possible model that captures the essence of the problem,” he said. “We often think of songbirds in a similar way. Birdsong is a very quantifiable behavior. Sensory motor learning is 50 percent or more of what brains are all about. It’s learning to integrate sensation and action to effectively control movements, in this case, vocalizations.”

Songbirds are known to form detailed sensory memories for their tutor songs, and to use the memories to guide the development of their own song to match the tutor over many months. However, until the new study there was no evidence for short-term memory of song that could form a substrate for more complex song rules.

Gardner and Yarden Cohen, then a postdoctoral student and the study’s lead author, began the fundamental research in Gardner’s Boston University lab before Gardner joined the Knight Campus in June 2019. Analyses of the data continued under Gardner’s tutelage after his arrival at the UO, where he also is affiliated with the Department of Physics.

“These birds produce songs that contain hundreds of syllables organized in a way that indicates that they are using the short-term memory of preceding song syllables to guide the choice of the next elements in song,” said Cohen, now a neurosurgery research fellow at Massachusetts General Hospital, which is affiliated with the Harvard Medical School.

“They create a complex syntax with long-range rules resembling properties of human behaviors like speech, dance and playing a musical instrument,” Cohen said. “We discovered that their song circuitry reflects the working memory required for their complex syntax.”

The research, Gardner said, delivers a new way to study the principles of short-term memory.

“If you reflect on the nature of speech, the choice of what to say next is guided by working memory that integrates over many timescales, from the overall aim of the communication episode to the local rules required for proper grammatical form,” Gardner said. “Canary song is much simpler, but it follows long-range syntax rules such as ‘sing syllable D’ only if five seconds ago I sang A rather than B.”

This deep structure, he said, contains simple similarities to speech where the ending of a sentence is dependent on how the sentence began. In both systems, correlations between past and future parts of the vocalization require a form of short-term memory.

“What is clear is that a lot of cellular rules that underlie learning and memory are highly conserved,” Gardner said. “For example, there are cells in the basal ganglia in songbirds that have incredibly similar patterns of activity to what has been seen in rodents. While brain architecture may differ, the fundamental computations expressed at a cellular level are the same.”

Gardner will continue to use the tools used in the study for his work in his Knight Campus lab. Ideally, he said, it could lead to not just to improved understanding of complex behaviors but also to enhanced machine-learning methods.

“A lot of what we see in the canary resembles computational models that have been used for speech recognition and general artificial intelligence algorithms,” he said. “Speech algorithms used in Siri and Google Assistant networks use these types of hidden states seen in the canaries.”

Eventually, Cohen said, studying the neural basis of canary song production may make it possible to understand how working memory mechanisms adapt to new conditions or fail when brain circuits are damaged. Developing such a model, he added, may point to new therapies for speech and comprehension deficits that come with aging and in neurodegenerative diseases such as Parkinson’s and Alzheimer’s.

Five grants from the National Institutes of Health supported the research team, which in addition to Gardner and Cohen included seven other members drawn from Boston University’s biology department and medical school.