Coding of vocalizations by single neurons in ventrolateral prefrontal cortex

Abstract

Neuronal activity in single prefrontal neurons has been correlated with behavioral responses, rules, task variables and stimulus features. In the non-human primate, neurons recorded in ventrolateral prefrontal cortex (VLPFC) have been found to respond to species-specific vocalizations. Previous studies have found multisensory neurons which respond to simultaneously presented faces and vocalizations in this region. Behavioral data suggests that face and vocal information are inextricably linked in animals and humans and therefore may also be tightly linked in the coding of communication calls in prefrontal neurons. In this study we therefore examined the role of VLPFC in encoding vocalization call type information. Specifically, we examined previously recorded single unit responses from the VLPFC in awake, behaving rhesus macaques in response to 3 types of species-specific vocalizations made by 3 individual callers. Analysis of responses by vocalization call type and caller identity showed that ∽ 19 % of cells had a main effect of call type with fewer cells encoding caller. Classification performance of VLPFC neurons was ∽ 42% averaged across the population. When assessed at discrete time bins, classification performance reached 70 percent for coos in the first 300 ms and remained above chance for the duration of the response period, though performance was lower for other call types. In light of the sub-optimal classification performance of the majority of VLPFC neurons when only vocal information is present, and the recent evidence that most VLPFC neurons are multisensory, the potential enhancement of classification with the addition of accompanying face information is discussed and additional studies recommended. Behavioral and neuronal evidence has shown a considerable benefit in recognition and memory performance when faces and voices are presented simultaneously. In the natural environment both facial and vocalization information is present simultaneously and neural systems no doubt evolved to integrate multisensory stimuli during recognition.

Responses of primate frontal cortex neurons during natural vocal communication

“…An additional 8 units exhibited a significant change in neural activity for both vocal-signal and vocal-motor portions of the behavior. Given that previous studies of rhesus monkeys (Gifford et al 2005;Plakke et al 2013a;Romanski et al 2005) and squirrel monkeys (Newman and Lindsley 1976) have all reported neurons responsive to vocalizations in the same areas of frontal cortex, the relatively weak sensory responses to vocal-signal stimuli across marmoset frontal cortex were somewhat surprising. Despite the weak responses to vocalization stimuli, we performed further analyses in parallel with vocal-motor responses to test whether effects at a population level might reveal key differences in neuronal patterns suggestive of why sensory responses were limited during this natural behavior.…”

“…One neocortical region that has undergone considerable change over primate evolution is frontal cortex (Semendeferi et al 2001), a substrate known to be involved in many complex aspects of human cognition and communication (Fuster 2008;Gabrieli et al 1998;Miller and Wallis 2012). Although aspects of communication signal processing in frontal cortex appear shared across humans and other NHPs (Averbeck and Romanski 2006;Cohen et al 2007;Gifford et al 2005;Plakke et al 2013a; Romanski and Averbeck 2009;Romanski et al 2005), the role of this neocortical substrate in NHP vocal production is more controversial. Much of the data on frontal cortex function during NHP vocal communication comes from studies of restrained animals (Averbeck and Romanski 2006;Cohen et al 2007;Gifford et al 2005;Romanski et al 2005).…”

Natural variability in species-specific vocalizations constrains behavior and neural activity

“…AL is part of the ventral auditory pathway; a pathway that is thought to mediate non-spatial sound perception (i.e., “what is the sound?”) (Bizley and Cohen, 2013; Plakke et al, 2013b; Rauschecker and Tian, 2000; Rauschecker and Scott, 2009; Romanski, 2004; Romanski and Averbeck, 2009). Consequently, neurons in different regions of this pathway have been tested for their sensitivity to vocalizations (Averbeck and Romanski, 2004, 2006; Cohen et al, 2007; Gaucher et al, 2013; Gifford et al, 2005; Kikuchi et al, 2010; Kusmierek and Rauschecker, 2009; Kusmierek et al, 2012; Perrodin et al, 2011; Petkov et al, 2008; Plakke et al, 2013b; Poremba et al, 2013; Romanski and Goldman-Rakic, 2002; Russ et al, 2008b; Tian et al, 2001). In particular, AL neurons respond robustly to specific vocalizations and, relative to other control stimuli, respond preferentially to vocalizations, (Kusmierek et al, 2012; Rauschecker and Tian, 2000; Russ et al, 2008b; Tian et al, 2001).…”

Neural correlates of auditory scene analysis and perception

“…Other areas show a greater degree of stimulus selectivity, such as neurons in the anterior portions of the temporal lobe, which are highly selective for individual vocalizations, and the voice of specific vocalizers. Finally, activity in the ventrolateral prefrontal cortex (vlPFC) seems to represent a processing stage beyond that of sensory processing since vlPFC activity reflects non-spatial auditory attention, auditory working memory, sound meaning, and multimodal sensory integration (Cohen et al, 2009; Gifford III et al, 2005; Lee et al, 2009a; Ng et al, 2013; Plakke et al, 2013a; Plakke et al, 2012; Plakke et al, 2013b; Poremba et al, 2004; Romanski et al, 2005; Romanski and Goldman-Rakic, 2002; Russ et al, 2008a; Russ et al, 2008b). …”