1. Posterior cingulate cortex, although widely regarded as a part of the limbic system, is connected most strongly to parietal and frontal areas with sensory, motor, and cognitive functions. To gain insight into the functional nature of posterior cingulate cortex, we have recorded from its neurons in monkeys performing oculomotor tasks known to activate parietal and frontal neurons. We have found that posterior cingulate neurons fire during periods of ocular fixation at a rate determined by the angle of gaze and by the size and direction of the preceding eye movement. 2. The activity of 530 posterior cingulate neurons was monitored while rhesus macaque monkeys made visually guided eye movements to spots projected on a tangent screen. 3. In 150/530 neurons, a statistically significant shift in the rate of discharge occurred around the time of onset of saccadic eye movements. The preponderant form of response was an increase in activity (142/150 neurons). 4. In 142 neurons exhibiting significant excitation after saccades in at least one direction, the level of discharge was analyzed as a function of time relative to onset of the saccade. Across the neuronal population as a whole, activity increased sharply at the moment of onset of the saccade, rising to a maximum after 200 ms and then declining slowly. The net level of discharge remained well above presaccadic baseline even after > 1 s of postsaccadic fixation. 5. In 63 neurons, the postsaccadic rate of discharge was analyzed relative to the angle of the eye in the orbit by monitoring neuronal activity while the monkey executed saccades of uniform direction and amplitude to four targets spaced at 16-deg intervals along a line. The postsaccadic firing level was significantly dependent on orbital angle in 44/63 neurons. 6. In 45 neurons, the postsaccadic rate of discharge was analyzed relative to saccade direction by monitoring neuronal activity while the monkey executed 16-deg saccades to a constant target from diametrically opposed starting points. The postsaccadic level of activity was significantly dependent on saccade direction in 20/ 45 neurons. 7. In 58 neurons, the postsaccadic rate of discharge was analyzed relative to saccade amplitude by monitoring neuronal activity while the monkey executed saccades, which varied in amplitude (4, 8, 16, and 32 deg) but which were constant in direction and brought the eye to bear on a constant endpoint. The postsaccadic level of activity was significantly dependent on saccade amplitude in 24/58 neurons. In all neurons exhibiting significant amplitude-dependence, stronger firing accompanied larger saccades. 8. The activity of 10 neurons was monitored during smooth pursuit eye movements (20 deg/s upward, downward, leftward, and rightward). The level of firing varied as a function of both the position of the eye (9 neurons) and the velocity of the eye (6 neurons). 9. We conclude that posterior cingulate neurons monitor eye movements and eye position. It is unlikely that they participate in the generation of eye movements because their shifts of discharge follow the onset of the movements. Eye-movement-related signals in posterior cingulate cortex may reflect the participation of this area in assigning spatial coordinates to retinal images.

The cingulate gyrus, encompassing Brodmann's areas 23, 24, 29, 30, and 31, is a major division of the cerebral cortical mantle found in all mammals including humans. As a large cortical district conserved across mammalian evolution, the cingulate gyrus might be expected to serve a clearly identifiable function, but the behavioral significance of cingulate cortex remains unclear. Theories of cingulate function that have been put forward rest, in large part, on indirect evidence, which includes the "paralimbic" connectional pattern whereby cingulate cortex is linked both to structures of the limbic system and to neocortical areas (Papez, 1937; MacLean, 1949; Mesulam, 1981; Pandya and Seltzer, 1982; Pandya and Yeterian, 1985).

The posterior cingulate cortex of the cat is strongly linked to cortical areas with sensory and oculomotor functions. We have now recorded from feline posterior cingulate neurons in order to determine whether they are active in conjunction with sensory events and eye movements. The results described here are based on monitoring the electrical activity of 195 single neurons in the posterior cingulate cortex of three cats equipped with surgically implanted scleral search coils and trained to fixate visual targets. Posterior cingulate neurons carry tonic orbital position signals and are phasically active in conjunction with saccadic eye movements. Activity related to eye movements and gaze is attenuated but not abolished by the elimination of visual feedback. Posterior cingulate neurons also are responsive to visual, auditory, and somatosensory stimulation. Systematic testing with visual stimuli revealed that responses are sharply reduced due to refractoriness at rates of stimulation greater than a few per second. These results conform to the theory that posterior cingulate cortex is involved in processes underlying visuospatial cognition.

The posterior cingulate area (CGp) of the cat consists of cortex on the exposed cingulate gyrus and in the adjacent ventral bank of the splenial sulcus. We have placed deposits of distinguishable fluorescent tracers at multiple restricted sites in CGp and have analyzed the distribution throughout the forebrain of neurons labeled by retrograde transport.Cortical projections to CGp arise (in approximately descending order of strength) from anterior cingulate cortex; prefrontal cortex and premotor areas including the frontal eye fields; visual areas including especially areas 7 and 20b; parahippocampal areas; insular cortex; somesthetic areas; and auditory areas. Corticocortical pathways are organized topographically with respect to the posterior-anterior axis in CGp. Projections from prefrontal cortex and other areas with complex (as opposed to sensory, motor, or limbic) functions are concentrated posteriorly; projections from visual and oculomotor areas are concentrated at an intermediate level; and projections from areas with somesthetic and somatomotor functions are concentrated anteriorly.Thalamic projections to CGp arise from the anterior nuclei (AD, AV, and AM), from restricted portions of the ventral complex (VAd, VAm, and VMP), from discrete sectors of the lateral complex (LD, LPs, and LPm), from the rostral crescent of intralaminar nuclei (CM, PC, and CL), and from the reuniens nucleus. Projections from AM, VAd, LD, and LPs are spatially ordered in the sense that more ventral thalamic neurons project to more anterior cortical sites. Projections from AV and AD are stronger at more posterior cortical sites but do not show other signs of topographic ordering. Projections from LPm, CM, PC, CL, and RE are diffuse.We conclude (1) that cortical afferents of CGp derive predominantly from neocortical areas including those with well established sensory and motor functions; (2) that limbic projections to CGp originate primarily in structures, including the hippocampus, which are associated with memory, as opposed to structures, including the amygdala, which are associated with emotional and instinctual behavior; and (3) that CGp contains subregions in which complex, ocular, or somatic afferents predominate.

The aim of these experiments was to establish the number and location of connectionally distinct areas in the medial frontal lobe of the cat. Thirty deposits of distinguishable retrograde tracers were placed at restricted sites spanning the medial frontal lobe in 16 cats. Following each deposit, the number of retrogradely labeled neurons in each of 17 thalamic nuclei was determined. Variations of the thalamic labeling pattern dependent on the location of the cortical tracer deposit were then analyzed by a quantitative procedure. The results indicate that the medial frontal lobe contains three fundamental divisions: the anterior cingulate area, medial area 6, and the medial prefrontal district. The anterior cingulate area derives its strongest thalamic input from the anteriomedial nucleus. Medial area 6 is the target of afferents originating in a dorsolateral sector of the mediodorsal nucleus and in the ventroanterior nucleus. Medial prefrontal cortex is heavily innervated by pathways originating in the core of the mediodorsal nucleus and in the principal ventromedial nucleus. Within each major district, thalamic connectional patterns exhibit graded regional variation, with the result that, whereas the connections of the district are not uniform, it is difficult to define further discrete subdivisions. We discuss these results in relation to previously proposed schemes for paracellation of the cat's medial frontal lobe and conclude that the infralimbic and prelimbic areas (areas 25 and 32) of previous systems are best understood not as discrete areas but as ventral and intermediate sectors of a continuous medial prefrontal domain.

The aim of the experiments reported here was to identify cortical and subcortical forebrain structures from which anterior cingulate cortex (CGa) receives input in the cat. Deposits of retrograde tracers were placed at nine sites spanning the anterior cingulate area and patterns of retrograde transport were analyzed. Thalamic projections to CGa, in descending order of strength, originate in the anteromedial nucleus, lateroposterior nucleus, ventroanterior nucleus, rostral intralaminar complex, reuniens nucleus, mediodorsal nucleus, and laterodorsal nucleus. Minor and inconsistent ascending pathways arise in the paraventricular, parataenial, parafascicular, and subparafascicular thalamic nuclei. The basolateral nucleus of the amygdala, the hypothalamus, the nucleus of the diagonal band, and the claustrum are additional sources of ascending input. Cortical projections to CGa, in descending order of strength, derive from posterior cingulate cortex, prefrontal cortex, motor cortex (areas 4 and 6), parahippocampal cortex (entorhinal, perirhinal, postsubicular, parasubicular, and subicular areas), insular cortex, somesthetic cortex (areas 5 and SIV), and visual cortex (areas 7p, 20b, AMLS, PS and EPp). In general, the limbic, sensory, and motor afferents of CGa are weak. The dominant sources of input to CGa are other cortical areas with high-order functions. This finding calls into question the traditional characterization of cingulate cortex as a bridge between neocortical association areas and the limbic system.

We have analyzed the cortical and subcortical afferent connections of the medial prefrontal cortex (MPF) in the cat with the specific aim of characterizing subregional variations of afferent connectivity. Thirteen tracer deposits were placed at restricted loci within a cortical district extending from the proreal to the subgenual gyrus. The distribution throughout the forebrain of retrogradely labeled neurons was then analyzed. Within the thalamus, retrogradely labeled neurons were most numerous in the mediodorsal nucleus and in the ventral complex. The projection from each region exhibited continuous topography such that more medial thalamic neurons were labeled by tracer from more ventral and posterior cortical deposits. Marked retrograde labeling without any sign of topographic order occurred in a narrow medioventral sector of the lateroposterior nucleus. Several additional thalamic nuclei contained small numbers of labeled neurons. In a subset of nuclei closely affiliated with the limbic system (the parataenial, paraventricular, reuniens, and basal ventromedial nuclei), retrograde labeling occurred exclusively after deposits at extremely ventral and posterior cortical sites. Within the amygdala, retrogradely labeled neurons occupied the anterior basomedial nucleus, the posterior basolateral nucleus, and a narrow strip of the lateral nucleus immediately adjoining the basolateral nucleus. The number of labeled neurons was greater after more ventral deposits. Very ventral deposits resulted in extensive labeling of the cortical amygdala. Within the cerebral cortex, the distribution of labeled neurons depended on the location of the tracer deposit. Comparatively dorsal deposits produced prominent retrograde transport to the anterior and posterior cingulate areas, to the agranular insula, and to lateral prefrontal cortex. Comparatively ventral deposits gave rise to prominent labeling of the hippocampal subiculum, various parahippocampal areas, and prepiriform cortex. On the basis of afferent connections, it is possible to divide the cat's medial prefrontal cortex into an infralimbic component, MPFil, marked by strong afferents from prepiriform cortex and the cortical amygdala, and a dorsal component, MPFd, without afferents from these structures. Further, within MPFd, it is possible to define an axis, running from ventral and posterior to dorsal and anterior levels, along which limbic afferents gradually become weaker and projections from cortical association areas gradually become stronger.