Daniel Bendor

The neuronal representation of pitch in primate auditory cortex

Pitch perception is critical for identifying and segregating auditory objects, especially in the context of music and speech. The perception of pitch is not unique to humans and has been experimentally demonstrated in several animal species. Pitch is the subjective attribute of a sounds fundamental frequency (f0) that is determined by both the temporal regularity and average repetition rate of its acoustic waveform. Spectrally dissimilar sounds can have the same pitch if they share a common f0. Even when the acoustic energy at f0 is removed (‘missing fundamental’) the same pitch is still perceived. Despite its importance for hearing, how pitch is represented in the cerebral cortex is unknown. Here we show the existence of neurons in the auditory cortex of marmoset monkeys that respond to both pure tones and missing fundamental harmonic complex sounds with the same f0, providing a neural correlate for pitch constancy. These pitch-selective neurons are located in a restricted low-frequency cortical region near the anterolateral border of the primary auditory cortex, and is consistent with the location of a pitch-selective area identified in recent imaging studies in humans.

Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys.

The core region of primate auditory cortex contains a primary and two primary-like fields (AI, primary auditory cortex; R, rostral field; RT, rostrotemporal field). Although it is reasonable to assume that multiple core fields provide an advantage for auditory processing over a single primary field, the differential roles these fields play and whether they form a functional pathway collectively such as for the processing of spectral or temporal information are unknown. In this report we compare the response properties of neurons in the three core fields to pure tones and sinusoidally amplitude modulated tones in awake marmoset monkeys (Callithrix jacchus). The main observations are as follows. (1) All three fields are responsive to spectrally narrowband sounds and are tonotopically organized. (2) Field AI responds more strongly to pure tones than fields R and RT. (3) Field RT neurons have lower best sound levels than those of neurons in fields AI and R. In addition, rate-level functions in field RT are more commonly nonmonotonic than in fields AI and R. (4) Neurons in fields RT and R have longer minimum latencies than those of field AI neurons. (5) Fields RT and R have poorer stimulus synchronization than that of field AI to amplitude-modulated tones. (6) Between the three core fields the more rostral regions (R and RT) have narrower firing-rate-based modulation transfer functions than that of AI. This effect was seen only for the nonsynchronized neurons. Synchronized neurons showed no such trend.

Differential neural coding of acoustic flutter within primate auditory cortex

A sequence of acoustic events is perceived either as one continuous sound or as a stream of temporally discrete sounds (acoustic flutter), depending on the rate at which the acoustic events repeat. Acoustic flutter is perceived at repetition rates near or below the lower limit for perceiving pitch, and is akin to the discrete percepts of visual flicker and tactile flutter caused by the slow repetition of sensory stimulation. It has been shown that slowly repeating acoustic events are represented explicitly by stimulus-synchronized neuronal firing patterns in primary auditory cortex (AI). Here we show that a second neural code for acoustic flutter exists in the auditory cortex of marmoset monkeys (Callithrix jacchus), in which the firing rate of a neuron is a monotonic function of an acoustic events repetition rate. Whereas many neurons in AI encode acoustic flutter using a dual temporal/rate representation, we find that neurons in cortical fields rostral to AI predominantly use a monotonic rate code and lack stimulus-synchronized discharges. These findings indicate that the neural representation of acoustic flutter is transformed along the caudal-to-rostral axis of auditory cortex.

Neural coding of temporal information in auditory thalamus and cortex (DOI: 10.1016/j.neuroscience.2008.03.065)

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate-based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representation in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate-based representations in the form of a monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of the marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.

Neural coding of periodicity in marmoset auditory cortex.

Pitch, our perception of how high or low a sound is on a musical scale, crucially depends on a sounds periodicity. If an acoustic signal is temporally jittered so that it becomes aperiodic, the pitch will no longer be perceivable even though other acoustical features that normally covary with pitch are unchanged. Previous electrophysiological studies investigating pitch have typically used only periodic acoustic stimuli, and as such these studies cannot distinguish between a neural representation of pitch and an acoustical feature that only correlates with pitch. In this report, we examine in the auditory cortex of awake marmoset monkeys (Callithrix jacchus) the neural coding of a periodicitys repetition rate, an acoustic feature that covaries with pitch. We first examine if individual neurons show similar repetition rate tuning for different periodic acoustic signals. We next measure how sensitive these neural representations are to the temporal regularity of the acoustic signal. We find that neurons throughout auditory cortex covary their firing rate with the repetition rate of an acoustic signal. However, similar repetition rate tuning across acoustic stimuli and sensitivity to temporal regularity were generally only observed in a small group of neurons found near the anterolateral border of primary auditory cortex, the location of a previously identified putative pitch processing center. These results suggest that although the encoding of repetition rate is a general component of auditory cortical processing, the neural correlate of periodicity is confined to a special class of pitch-selective neurons within the putative pitch processing center of auditory cortex.

Enhance, delete, incept: Manipulating hippocampus-dependent memories

Highlights • Newly developed methods allow manipulation of hippocampus-dependent memories.• Cued reactivation during sleep and transcranial stimulation can enhance memories.• Pharmacological agents can delete memories.• Optogenetics and DREADDs can be used to incept memories.• Electrophysiology and fMRI have been used to investigate the underlying mechanisms.

Global timing: a conceptual framework to investigate the neural basis of rhythm perception in humans and non-human species.

Timing cues are an essential feature of music. To understand how the brain gives rise to our experience of music we must appreciate how acoustical temporal patterns are integrated over the range of several seconds in order to extract global timing. In music perception, global timing comprises three distinct but often interacting percepts: temporal grouping, beat, and tempo. What directions may we take to further elucidate where and how the global timing of music is processed in the brain? The present perspective addresses this question and describes our current understanding of the neural basis of global timing perception.

Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs

The hippocampus is critical for the storage of new autobiographical experiences as memories. Following an initial encoding stage in the hippocampus, memories undergo a process of systems-level consolidation, which leads to greater stability through time and an increased reliance on neocortical areas for retrieval. The extent to which the retrieval of these consolidated memories still requires the hippocampus is unclear, as both spared and severely degraded remote memory recall have been reported following post-training hippocampal lesions. One difficulty in definitively addressing the role of the hippocampus in remote memory retrieval is the precision with which the entire volume of the hippocampal region can be inactivated. To address this issue, we used Designer Receptors Exclusively Activated by Designer Drugs (DREADDs), a chemical-genetic tool capable of highly specific neuronal manipulation over large volumes of brain tissue. We find that remote (>7 weeks after acquisition), but not recent (1–2 days after acquisition) contextual fear memories can be recalled after injection of the DREADD agonist (CNO) in animals expressing the inhibitory DREADD in the entire hippocampus. Our data demonstrate a time-dependent role of the hippocampus in memory retrieval, supporting the standard model of systems consolidation.

Does the Hippocampus Map Out the Future

Decades of research have established two central roles of the hippocampus--memory consolidation and spatial navigation. Recently, a third function of the hippocampus has been proposed: simulating future events. However, claims that the neural patterns underlying simulation occur without prior experience have come under fire in light of newly published data.

The Role of Inhibition in a Computational Model of an Auditory Cortical Neuron during the Encoding of Temporal Information

In auditory cortex, temporal information within a sound is represented by two complementary neural codes: a temporal representation based on stimulus-locked firing and a rate representation, where discharge rate co-varies with the timing between acoustic events but lacks a stimulus-synchronized response. Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition. In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition. Using single-unit recordings from awake marmosets (Callithrix jacchus), we validate several model predictions, including differences in the temporal fidelity, discharge rates and temporal dynamics of stimulus-evoked responses between neurons with rate and temporal representations. Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.