Representation of the purr call in the guinea pig primary auditory cortex
Introduction
Naturally occurring vocalizations are being increasingly used as probes with which to understand the processing of complex sounds by the cortex. Studies in the macaque monkey have led to the suggestion that there may be separate pathways for analyzing the spatial location of sound sources within auditory space and the significance of sounds such as conspecific calls (Tian et al., 2001). Behavioural studies of their significance have suggested that some primates can encode information about their own identity, species, sex, motivational state and size by variations in one type of call and information about surrounding objects such as the quality of food or the type of predator by other types of call (Ghazanfar and Hauser, 2001). Semantic information of this type may not be restricted to primate calls, but is also present in the calls of rodents, with a well-developed social organization, such as Gunnison’s prairie dogs (Slobodchikoff et al., 1991) or red squirrels (Greene and Meagher, 1998). In an attempt to try and understand how the cortex could code the information within calls, some workers have recorded from many locations along the tonotopic axis of the primary auditory area (AI), during the presentation of many different examples of the same vocalization, in order to study the neural classification of different examples of a call. Thus, cortical recordings made in the marmoset (Wang, 2000, Nagarajan et al., 2002) and squirrel monkeys (Bieser, 1998) have allowed the determination of the spectral and temporal parameters which underlie the classification of the same as well as separate types of call.
An alternative approach is to present one sample vocalization to many neurones within a restricted frequency range of AI that coincided with the main frequencies of the call. As most of the sound energy contained in the purr is in the frequency range of 270–1000 Hz, this allowed us to make detailed sampling within a relatively small number of isofrequency bands. It also allowed us to look for evidence of intracortical processing and for systematic differences in the response across the different layers of the cortex. As these were experiments aimed at learning more about basic cortical processing a common laboratory animal was deemed appropriate.
Guinea pigs have a well-developed social organization in the wild and the domesticated form (Cavia porcellus) are very vocal mammals with a repertoire of at least 11 different communication calls that have been grouped into 6 classes by Berryman (1976). The “purr” class is the least variable of all the guinea pig calls and contains two structurally similar calls named the “drrr” and “purr”. The purr used in this study corresponds to the drrr of Berryman (1976) and the alarm rumble described by Rood (1972) and Arvola (1974). It seems to be used as an alerting signal and causes all nearby animals to stop moving and sometimes respond with a purr of their own (Berryman, 1976). The drrr lasts from 200 to 800 ms and contains 4–11 separate pulses. It is structurally similar to the “rut rumble” or purr that is associated with mating behaviour except that these calls typically last at least 5 times as long. Purrs from females were often found to contain higher harmonics than those from males, but it is not known if these differences are used in identifying the sex of another animal.
In a previous study of phase-locked responses to pure tones in guinea pig AI, we showed that some of the phase-locked cells gave very strong responses to an example of purr, which accurately reflected the fine temporal structure of the call (Wallace et al., 2002b). By contrast, in other units the response to purr was much weaker or insignificant (Wallace et al., 2000b). An earlier study of responses to vocalizations involved simultaneous recordings from correlated cells in the guinea pig cortex and thalamus. This suggested that cortical cells were unable to follow the waveform envelope of a call as accurately as thalamic cells (Creutzfeldt et al., 1980). We did not attempt simultaneous recordings, but also recorded the response to purr shown by thalamic cells to compare them to cortical responses. In order to look for differences in the cortical response along an isofrequency band, we used tangential tracks oriented parallel to their long axis and we also used orthogonal tracks to study interlaminar differences at one cortical locus.
Section snippets
Surgical preparation
A total of 44 pigmented guinea pigs of both sexes and weighing 398–900 g contributed to this and other studies. In 20 animals anaesthesia was induced by injections of ketamine hydrochloride (60 mg/kg s.c.) and xylazine hydrochloride (Rompun™) at 16 mg/kg xylazine (i.m.) followed by supplementary doses of 15 mg ketamine hydrochloride (i.m.) as required to achieve abolition of the forepaw withdrawal reflex. Thereafter a mixture of 15 parts ketamine: 2 parts xylazine was administered (i.m.)
Population responses to purr
The exemplar of purr used in this study contained nine regular phrases within a period of about 670 ms (Fig. 2). These phrases varied in amplitude with the first 3 lower in level than the last 6. The phrases also varied in rise time and although they occurred at regular intervals each had a distinctive waveform envelope. The frequency components were more similar as each had a fundamental frequency at 270–315 Hz and none contained significant energy at frequencies above 1100 Hz. Consequently only
Cortical representation of individual calls
There have been no previous systematic studies of the cortical responses to conspecific calls in the guinea pig. However, previous studies had used the purr call in addition to other stimuli and showed that the purr could produce faithful representations of its multiple phrases in some cells within AI (Wallace et al., 2002b). In behavioural terms, the purr is a very important call for the guinea pig because the extended form of the call (rut rumble) is important in the mating ritual while the
Acknowledgments
We thank Prof. J. Syka for providing us with digitised recordings of the guinea pig purr.
References (34)
- et al.
Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls
Hear. Res.
(2000) - et al.
The auditory behaviour of primates: a neuroethological perspective
Curr. Opin. Neurobiol.
(2001) - et al.
Red squirrels, Tamiasciurus hudsonicus, produce predator-class specific alarm calls
Anim. Behav.
(1998) - et al.
Functional convergence of response properties in the auditory thalamocortical system
Neuron
(2001) - et al.
Organisation of binaural interactions in the primary and dorsocaudal fields of the guinea pig auditory cortex
Hear. Res.
(2000) - et al.
Semantic information distinguishing individual predators in the alarm calls of Gunnison prairie dogs
Anim. Behav.
(1991) - et al.
Phase-locked responses to pure tones in the primary auditory cortex
Hear. Res.
(2002) Vocalization in the guinea-pig, Cavia porcellus L
Ann. Zool. Fennici.
(1974)Guinea-pig vocalizations: their structure, causation and function
Z. Tierpsychol.
(1976)Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys
Exp. Brain Res.
(1998)
Thalamocortical transformation of responses to complex auditory stimuli
Exp. Brain. Res.
Syntax processing by auditory cortical neurons in the FM-FM area of the mustached bat Pteronotus parnellii
Proc. Natl. Acad. Sci. USA
Functional architecture of macaque monkey visual cortex
Proc. R. Soc. Lond. B
Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates
J. Neurophysiol.
Directional statistics
Glass-coated platinum-plated tungsten microelectrodes
Med. Biol. Eng.
Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat
J. Comp. Neurol.
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2011, Hearing ResearchCitation Excerpt :This showed that the artificially manipulated versions of the call were just as effective a stimulus as the original call (281 Hz) and indeed were more effective. Our previous study of purr responsive neurons in AI had been restricted to the low-frequency end (≤3 kHz) (Wallace et al., 2005b). However purr responses have been described in 40% of units with CFs of 16–32 kHz in the inferior colliculus (Šuta et al., 2003) and in thalamic units with CFs of up to 15 kHz (Šuta et al., 2007).
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2011, Hearing ResearchCitation Excerpt :The rhythmic structure of the sound bursts in the purr call may also be important in permitting a prolonged time-locked response because recent work in the ferret has shown that the temporal envelope of a complex sound may act in gating the analysis of fine structure at up to a few hundred Hz (Elhilali et al., 2004). We have previously suggested that the responses to the purr stimulus are organized in a columnar fashion (Wallace et al., 2005; Wallace and Palmer, 2009) and our previous results (Wallace et al., 2002) indicate that there is at least a partial overlap between the cells that phase-lock to pure tones and those that accurately represent the structure of the purr. However, there is not a one-to-one correspondence as we were able to record units that gave a strong, time-locked response to the purr call but did not phase-lock to pure tones.